Psychologische Forschung 31, 299--337 (1968)
Two Mechanisms of Vision in Primates *
COLWYN :B. TREVA~THE~
Center for Cognitive Studies, Harvard University
Received January 15, 1968
Zusammen]assung. Versuche an ,,split-brain" Allen legten die Annahme nahe,
daft die Wahrnehmung des Raumes und die Wahrnehmung der Identit~t yon Gegenst~inden ~uf anatomisch getrennten ttirnmechanismen beruhen. In der vorliegenden
Arbeit werden die Sehmeehanismen des Gehirns untersucht, wobei yon der ~berlegung ausgegangen wird, dab hier zwei parallele Prozesse involviert sind: ein dezentrierter (,,ambient"), der die Wahrnehmung des den K5rper umgebenden Raumes
bestimmt, und ein zentrierter (,,focal"), dureh welchen Details kleiner Raumfl/~chen
aufgefaBt werden.
Bei Wirbeltieren wird eine detaillierte Topographic des kSrper~zentrierten
Verhaltensraumes vom Auge zum Mittelhirn projiziert. Diese visue]le Topographie
ist so mit dem bi-symmetrischen motorischen System integTiert, dab sich eine Korrespondenz zwisehen gesehenen Punkten und Bewegungszielen ergibt.
Das phylogenetisch jiingere visuelle System des Vorderhirns befal3t sich fast
ausschliel31ich mit dem zentralen Verhaltensraum; die corticale motorische Kontro]le befaBt sich entsprechend mit sehr spezifischen Handlungen im gleichen
zentralen Gebiet.
Anatomic und Hirnchirurgie liefern bei Primaten ttinweise auf einen visuellen
Mechanismus im Mittelhirn, der flit die dezentrierte Raumwahrnehmung eine Rolle
spielt. Im Gegensatz dazu greift das auf Fovea, Parafovea und den visuellen Arealen
des Cortex beruhende zentrierte Sehen Areale des umgebenden Feldes fiir eine
eingehendere Inspektion heraus. Koordinierte Augenbewegungen sind direkter
Ausdruck dieser Aufmerksamkeitszuwendung.
Die Wechselwirkung zweier Meehanismen der visuel]en Analyse kennzeichnet
das Sehen bei allen aktiven Tieren. Die Komplexit/it des zentrierten Sehens zeigt
sich auf allen Stufen des visue]len Systems yon Primaten und in den Teilen des
motorisehen Systems, welehe das Sehen ausrichten und die auf bestimmte visuelle
Objekte gerichteten Itandlungen steuern.
Summary. Experiments with split-brain monkeys led me to consider that vision
of space and vision of object identity may be subserved by anatomically distinct
brain mechanisms. In this paper I examine the visual mechanisms of the brain to
test the idea that vision involves two parallel processes; one ambient, determining
space at large around the body, the other/ocal which examines detail in small areas
of space.
In vertebrates there is a projection from eye to midbrain of a detailed topography
of body-centered behavioral space. This visual map is integrated with the bisym* The preparation of this manuscript was supported in part by Grant No. 1
PO1 MH 12623 from the National Institutes of Health to Harvard University,
Center for Cognitive Studies, and in part pursuant to a contract, OE 6--10--043,
with the United States Department of Health, Education and Welfare, Office of
Education, under the provisions of the Cooperative Research Program, while the
author was a Research Fellow at the Center.
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C.B. TREvA~THEN:
metric motor system to obtain correspondence between visual loci and the goals
for movements. The midbrain visual system governs basic vertebrate locomotor
behavior.
The phylogenetically more recent forebrain visual system looks almost exclusively at central behavioral space, and cortical motor control is likewise concerned
with the formulation of highly specific acts in the same central territory.
Anatomy and brain surgery reveal a midbrain visual mechanism in primates
which plays a part in ambient space perception over the whole field. In contrast,
focal vision served by the fovea and parafovea and by the cortical visual areas picks
out areas in the ambient field for close attention. Conjugate eye movements are
the most direct sign of this attention.
The interplay between the two channels of visual analysis is a feature of vision
in all active animals; but the complexity of focal vision in primates is revealed in
their visual system at all levels, and in the parts of the motor system which orient
vision, or which govern acts directed to specific visual objects.
Introduction
M y i n t e r e s t in a d i s t i n c t i o n b e t w e e n vision of space a n d vision of
things or i d e n t i t i e s d a t e s from e x p e r i m e n t s in which I f o u n d t h a t a
split-brMn m o n k e y is capable of double perceiving a n d learning for some
visual stimuli, b u t n o t for others (TI~EVAI~TI~1~N, 1962a, 1962b, 1965).
A split-brMn s u b j e c t has all neural cross-connections b e t w e e n t h e cerebral
cortices c u t and, in addition, t h e optie e h i a s m a is d i v i d e d to o b t a i n
s e p a r a t e aceess of visual m a t e r i a l to each cortex. E x p e r i m e n t s w i t h b o t h
m o n k e y s a n d m a n h a v e shown t h a t when t h e hemispheres are disconn e c t e d t h e s e p a r a t e d cortices m a y perceive, l e a r n or t h i n k i n d e p e n d e n t l y .
I n m y e x p e r i m e n t s I f o u n d t h a t m o s t b u t n o t all processes were
d i v i d e d b y t h e operation, a n d t h e w a y in which p e r c e p t i o n of stimuli
segregated into "split" a n d "not s p l i t " suggested t h a t "thingness"
versus " d i f f e r e n c e in d e g r e e " was involved. Conflicting choices were
easily a c q u i r e d b y two s e p a r a t e cortical s y s t e m s when t h e stimuli to be
distinguished were, to me, quite unlike in k i n d so t h a t I could easily
n a m e t h e m ; for example, " c r o s s " versus " c i r c l e " . On t h e o t h e r h a n d ,
those stimuli for which subcortieal i n t e r a c t i o n s occurred during double
learning a p p e a r e d to be like in k i n d - - b u t somehow differently p l a c e d
w i t h i n a c o n t i n u u m or series; for e x a m p l e , " f i v e - p o i n t e d s t a r " versus
"six-pointed s t a r " , "dim" versus "bright", "orange" versus " c o m p l e m e n t a r y b l u e " . I t was n o t s i m p l y a m a t t e r of s i m p l i c i t y of t h e stimuli
or "easiness" of distinguishing b e t w e e n t h e m . I~ather, each one of t h e
second k i n d of s t i m u l i could be i m a g i n e d t r a n s f o r m e d into its p a r t n e r
b y a single function, in t h e w a y t h a t an o b j e c t m a y be t r a n s f o r m e d in
visual a p p e a r a n c e w h e n i t m o v e s a b o u t in space.
Could i t be t h a t two different visual m e c h a n i s m s were involved, one
h i g h l y eorticalised a n d distinguishing things like crosses a n d circles,
t h e o t h e r p a r t l y " b r a i n s t e m , " distinguishing o t h e r k i n d s of s t i m u l u s
Two Mechanisms of Vision in Primates
301
features, and adapted to making comparisons between spatially separated
configurations or areas ? There was an anatomical question leading to
consideration of midbrain visual functions in the monkey, functions
which seemed to me to be poorly understood in the literature. There was
also the hint of a functional differentiation between two kinds of vision,
at ]east partly related to midbrain-forebrain differences.
I n a follow-up experiment, I found t h a t I could force the two hemispheres of a monkey with forebrain split to compare the sizes of circles
placed about 20 ~ apart in a horizontally aligned pair (TnEvA~T~E~,
1963). Again, b y some kind of vision capable of determining relative
size, the subject could compare or weigh against one another these
slightly different stimuli which were seen in opposite halves of the visual
field and presumably in opposite halves of the brain.
Before presenting these experiments in detail and an interpretation
of them, I should like to go over the fruits of m y attempts to find the
biological significance, ff any, of a distinction between vision of relationships in an extensive space and visual identification of things.
I n order to think about visual perception as a brain process, it is
necessary to consider the relationship between perception and voluntary
motor functions. Vision takes place in a brain which is capable of specflying acts according to the contents of vision. I n the process, vision
reproduces neither the pattern of retinal stimulation nor the physical
events of which this pattern is an image. I t is more closely attuned to
physical events in the sense t h a t the pereeiver's predictions for action
must conform to the physical world. Transformations in the perceptual
representation of the physical world are always related to the capacity
which the perceiver has for action. Consider the phenomenon of size
constancy from this point of view: a seen object has ultimate utility in
so far as it is seen accurately where it is in space and what size it would be
ff it were close enough to be seized, spoken to, and so forth. Visual perception and the plans for voluntary action are so intimately bound together
t h a t they m a y be considered products of one cerebral function.
We are asking ff this integrative function involves the combined
action of two components - - two mechanisms of visuo-motor integration.
If so, the distinction of two visions should carry through to define two
kinds of action or movement, each with its own visual afferent frame.
Animals act as though they were continuously cognizant of a space
for behavior around the body. Their actions are precisely the right size
and the right speed and are made at the right time to fit events and
selfmade changes in the world surrounding them. I n this world, acts are
made from the body as center and origin. Therefore, the spatial frame for
activity has a s y m m e t r y imposed upon it; it is bisymmetric with the
midplane of the body and polarized in the antero-posterior direction of
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C.B. TREVARTHEN:
the body axis. I shall call this body-centered space the behavioral space.
Acts are defined as directed towards goals in it, and percepts governing
acts are "located" in it.
There are, indeed, two main kinds of acts made in the behavioral
space, and each has its own dependency upon visual afference for guidance and confirmation. Orientations of the head, postural adjustments,
locomotor displacements change the relationship between the body and
spatial configurations of contours, surfaces, events, and objects. These
movements occur within what I shall call ambient vision. In contrast,
praxic actions on the environment to use pieces of it in specific ways are
performed with the motor apparatus of the body and the visual receptors
oriented together so that both vision and the acts inflicted on the environment occur in one part of the behavioral space. The vision applied to
one place and a specific kind of object, or deployed in a field of identified
objects, I shall call ]ocal vision. I t is this examining and identifying kind
of vision, serving refined and discriminating acts, which has evolved to
quite a new level of proficiency and complexity in primates, especially
in man.
l~rimate Visual Behavior
Behavior in Ambient Visual Space
To walk or climb, to fight, to do heavy work, a fast-moving animal
must perceive a wide three-dimensional field near the body, and must
differentiate the solidity, continuity, spatial separation and mobility of
objects in it. I t would appear that such differentiations are made instantaneously by visual perception of wide scope, but with relatively
crude capacity to discriminate detailed features of objects.
Primates are agile within complex visual fields. Presumably the
arboreal habitat of early primates imposed selective pressure which
favored the evolution of vision resolving three-dimensional space from
fast-changing retinal images. During large movements displacing the
eyes, the three-dimensional arrangement of objects in the surrounding
world is signalled in transformations of the retinal image. When the eyes
move forward, the largest image motions occur on the nasal retinae onto
which the lateral (temporal) fields are projected (Fig. 1). The eyes of
primates are frontally oriented and, as a result of this, the lateral monocular parts of the field constitute only about one half of the total field
(Fig. 2). The characteristics of the kind of vision employed in the regulation of large scale acts may be best seen in these lateral parts of the
field. As is clear from Fig. 2, their extent is adapted to visual guidance
of the limbs and body in walking or climbing.
Vision in the lateral fields remains efficient in low light, is highly
sensitive to motion, and produces little impression in consciousness. Thus,
Two Mechanisms of Vision in Primates
303
climbing or running over rough ground may be skillfully executed in
moonlight with only scotopie vision, i scarcely attend to the motion
effects at the peripheral part of the visual field; nevertheless, this part
provides me with very reliable information about nearby bulks and
surfaces as I walk about or when I am reaching for objects to the side
OcuLOMOTOR SACCADEs
/
Fig. 1. The visual field of the right eye of man at the horizontal meridian. A Relative visual acuity. Based on W~RT~I3~ (1894) and W~Y~rouTtr (1958). B The
retinal displacement vectors for objects at equal distance from the eye when the
eye moves forward a given distance along its axis. C Relative frequencies of rods
(large dots) and cones (small dots) (OsT~RB~G, 1935). M Anterior border of the
monocular temporal crescent
of where I am looking. I t is m y impression that, during large, continuous
displacements of m y body, central acuity is greatly reduced, as if the
whole visual field has become dispersed or extended rather than peaked
about the fovea, and then the central part of the visual field has
functions approaching those characteristics of the lateral parts. The
same equalizing of functions over the visual field occurs when scotopic
conditions prevail.
The primitive living primates are predominantly nocturnal with
specializations for seotopic vision (B~YETT~S~-JA~YSCH, 1963). The
]oruses and some lemurs are active on starlit and moonlit nights, or at
dusk, and leap and run in tropical forest trees. The Galago captures
304
C.B. T~EV~.~THE~:
small movixlg insects in moonlight with rapid, snatching movements of
the hands ; it is probable that vision is as important as acute audition in
governing this feat (BishoP, 1963). The nocturnal prosimians appear to
be supreme masters of ambient vision.
/
//
'/
/
/
//
Fig. 2. The visual field of man. A Seated at work. The field is oriented and drawn
close to provide focal vision for the hands and objects manipulated. B Walking or
standing and fixating a small near object, or the face of a distant person. Ambient
vision provides information about space, especially during forward progression.
Focal vision is applied to a close or far object of attention. C Locomotion among
obstacles and over irregularities. The gaze is cast down. This extends the range of
ambient vision for control of wMking. Focal vision is applied to detail of the terrain
Praxic Behavior and Focal Vision
While the nocturnal prosimians are agile at climbing and catching
small animals, their praxic behavior is rudimentary compared with that
of higher primates (NAPI~a, 1956, 1960; BISHOP, 1963). The latter are
active by day, and they have well-developed color vision of high acuity
and, in addition to their skillful locomotion, they perform delicate
manipulations of small objects while seated, oriented to the task (Fig. 2).
I n association with the evolution of manipulatory behavior, the primates
make spontaneous eye movements which are of unique freedom and
complexity; they are the only mammals with well-developed foveae
(Fig. 1). There is a consistent relationship :in the evolution of vertebrates
between spontaneous space-sampling eye movements and the appearance
Two Mechanisms of Vision in Primates
305
of optical and retinal specializations favoring heightened visual analysis
at a center of regard (WALLs, 1942, 1962).
A monkey or a man m a y make saccadic shifts of regard up to 90 ~ off
center by rapid rotations of head and eyes, and in this way he obtains a
clear perception of the world in front of him from a succession of
spatially discrete samples. Primates are, in fact, the only animals which
habitually explore a relatively wide segment of the visual field with
saccadic eye movements while the head is kept in constant orientation.
With the attainment of a much higher capacity for processing detailed
visual information, they show a refined oculomotor sampling behavior.
I n man, only the eyes move to explore a frontal area which subtends
about 45~ to look at points outside this central zone of the behavioral
field, the head moves with the eyes in a precisely coupled manner
(Fig. 1). The saccadic eye movements are quite different in function
from the other kinds of spontaneous or voluntary movements of the
eyes relative to the outside world, such as those which are occasioned
by voluntary approach of the body to a point in locomotor space, or
voluntary re-orientation of the head and eyes. When m y eyes move, I experience a heightened resolution of part of the field at each fixation.
I do not, however, see the jumps across the field, and I am not aware of
m y eye movements, nor can I see them in a mirror. Even the order of
attention to points escapes me. With accumulation of m a n y focal samples, I experience a building and extending of clarity in vision of the part
of the visual world in front of me.
A monkey or a man changes the strategy of saccadic exploration
depending upon the fa.miliarity of the surroundings, his goals, and his
state of excitement or apprehension. The strategy is closely attuned to
the structure of the spatial array, for example, an open savannah where a
lion m a y be. H u m a n subjects employ their foveal vision with careful
choice of particular parts of the visual space in front of them. They
explore a picture intelligently, endowing it with spatial structure
(YAI~]~VS, 1967).
While the intake or rejection of visual information from the world
is regulated b y these rotations of the eyes and by movements of the lids,
iris, and lens, a primate also shows special motor refinements in his
capacity to act within the visible world, to bring him into new physical
contact with it, to change it, to absorb it, or to destroy it to his advantage. The higher monkeys and men spend a large part of their time
seated or standing bipedally, oriented to a task, their visual attention
absorbed in a small part of space (Fig. 2). Then the central 60 ~ of good
stereoscopic vision is under easy and rapid surveillance b y the flickering
conjugate eye movements which aim the fovea. Either hand m a y be
placed anywhere close in this territory for precisely formed and timed
306
C.B. TI~EVAt~TI:[E~:
actions. This is where critical perceptual experience is acquired and
where m a n y skills are elaborated.
When attention is concentrated to a small, near part of the world,
or to a far distant object or event, the body is immobilized, and the head
and eyes are kept in fixed orientation so t h a t only small saccadic displacements of regard need be made. Fixation is broken only if the
observed object is making predictable, fairly slow motion. I n this ease,
tracking movements, "object-holding" or "field-holding" movements, as
WALLS (1962) calls them, underlie fixation. Similar fixation accompanies
the finest manipulatory work in which only one or two fingers m a y move.
Wrist, arm and shoulders provide an immobile support or a smoothly
moving supporting frame. Mobile fixation also accompanies elaborate
facial and vocal communications of monkeys and man.
This brief survey of primate behavior provides us with information
about vision of ambient space and vision of particular things isolated
in space. Viewed broadly, the visual behavioral space of the primate
does appear to have two components.
Laterally, there are two monocular visual fields, each selectively sensitive to change or motion; they form the marginal parts of an ambient
orientation frame which extends throughout the visual field. Within this
frame, vision resolves detail down to a degree or two and is threedimensional, but it is poor for discrimination of local features. Each
monocular field is in range for movements of only one hand.
I n front of the head is the binocular central field in which focal
vision is served by foveal resolution of detail and hue and where fine
depth separations are detected stereoptically. Exploratory eye movements are essential to focal vision within the central part of the visual
field, and, in this territory, nearby visible objects are grasped b y the
hands to be manipulated bimanually, or to be transported to the mouth.
I t should not be concluded that, because these two modes of vision
are distinct peripherally, they are independent within normal visual perception. They are complementary, and both are involved in the visual
regulation of behavior at any moment. Information about the space and
the motion of parts within the ambient field provides the contextual
information for the ordering of focal perception within the central part
of the field. There is, thus, a reciprocal partnership between focal
vision served b y the fovea and vision in the parafoveal zones of the
central field in which the fovea is placed in central scanning. There is
also a reciprocal interaction between the central binocular fields and
the far peripheral fields in control of large scale orientations of the
individual as a whole. These interactive relationships are discussed
further below.
Two Mechanisms of Vision in Primates
307
Brain Mechanisms of Ambient and Focal Vision in Primates
The main features of the eyes, eye muscles and locomotor apparatus
of vertebrates were evolved early in their history, and they have been
retained throughout. I n the brains of vertebrates, the visuo-motor
mechanisms associated with these structures are homologous. All vertebrates possess direct projections from the eyes to a laminated cortex-like
field in the anterior midbrain roof, the optic rectum. Other fibers or
collaterals also pass to the pretectum and to the posterior diencephalon,
the optic thalamus. The oculo-motor nuclei are in the ventral midbrain,
and the efferent projections of the rectum are principally concerned
with regulation of orienting movements involving the eyes, trunk, and
limbs in concerted action.
I n reptiles and mammals, the forebrain cortex receives fibers in a
secondary relay from the diencephalon. Rodents have a small visual
cortex and so do shrews, but it is much larger in highly visual and aggressively mobile mammals, such as a cat or a monkey or a man. In primates,
the occipital (visual) cortex is so large t h a t it both physically and functionally overshadows the inidbrain visual system. I n consequence, we
know next to nothing about the superior colliculus of primates.
Topographic Projections o/ Visual Space
Body-centered visual space has a representation in a remarkably
precise map-like distribution of visual points over the surface of the
rectum in every vertebrate which has been mapped. The m a p is highly
consistent throughout the group, in spite of variation in the geometry
and in fine a n a t o m y of the eyes and the central visual mantle, and it is
independent of the fact t h a t the eyes are variously aligned with the
body axis in different forms. This precise topographic organization of
neurone connections would appear to reflect a fundamental consistency
in what the mid-brain of vertebrates is designed to do.
The superior colliculi of a variety of vertebrates are shown in Fig. 3.
The brains in outline show the changing proportions of the basic parts.
The map of the visual behavioral frame on the rectum is plotted, first in
the optical coordinates of the eye, and second in the coordinates of the
behavioral field; i.e., with respect to the s y m m e t r y of the body. The data
for these maps has been accumulated recently b y histological, behavioral,
and electrophysiological techniques 1.
Many of these maps were originally represented on the optical
coordinates of the eye, a procedure which leads to a variety of
1 The electrophysiological maps are the most precise. The most complete maps
are as follows: Goldfish: S c ~ w A s s ~ and K~Gn~ (1965); Frog: JAcoBso~
(1962), G_~z~and J~COBSO~-(1962); Rat: SIMI~GFF, SC~WASS~A~ and K ~ v G ~
(1966); Cat: AP~ER (1945).
308
C. B . T R E V A R T H E N :
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Fig. 3. Colliculus maps in several vertebrates. 0 optical axis; L lateral genicu]ate
(and other visual nuclei of dorsal thalamus); P pretectum; C optic rectum
superior collieulus; h and v horizontal and vertical meridia of the optical visual
field; H and V horizontal and vertical meridia of the body-centered behavioral
visual field. The shaded line on the right tectum indicates the border of the binocular
field. The striate areas of the cortex are shown for the rat and cat with the central
or foveal areas in black. The dotted areas of cortex are also implicated in visual
functions
projections t h a t do n o t look very similar. The b r a i n does n o t keep a fixed
relationship to the geometry of the optical system of the eye as such.
More consistent are the maps i n "behavioral" coordinates. These m a p s
depict the space of visual goals for m o v e m e n t s produced with respect
to the b o d y axis b y a b i s y m m e t r i c m o t o r system. A centering m o v e m e n t
Two ~r
of Vision in Primates
309
in this space brings an object toward the horizontal meridian and along
it to the behavioral center in front of the animal. I t is significant t h a t the
central part of the behavioral field where consummatory acts are performed is represented rostrally, adjacent to other visual zones, the pretecturn and dorsal thalamus, the latter of which projects to the cortex. The
binocular fields, which vary, are placed on the rostro-medial edge of the
colliculus. The monocular, temporal fields are well represented; even in
the cat, with frontally-oriented eyes, only about half of the projection
is occupied by the binocular field.
There are no adequate data published for the primate tectal map, so,
in its absence, we assume t h a t it would fall in line with the other vertebrates.
Stimulation experiments have shown t h a t this m a p of visual points
does, indeed, also m a p a topography of points of entry to a motor
mechanism which produces appropriate orientation movements, bringing
objects into behavioral control. I t is not merely a sensory topography.
AKE~T (1949a, b) stimulated the rectum of trout and produced orienting
reactions of the eyes and the trunk and fins, as if the fish were turning
to an object in the corresponding half of visual space. A P T ~ (1946) made
precise observations with the cat, showing t h a t a m a p of ocular orientations to points in the space outside the body m a y be plotted on the surface of the rectum, and t h a t this and the map of the visual projections
from the same space are in register. H e r observations have been confirmed by ItYD~ and ELIASSO~ (1957). When the cat is not restrained in
a stereotaxic machine and is free to make general body movements,
stimulation in the rectum and adjacent reticular formation produces
a combined orientation of eyes, head and trunk varying according to the
duration and intensity of stimulation. Comparable eye movements in
monkeys under brain stem stimulation or after brain stem lesions are
described b y B ] ~ D ~ and SKA~Z~ (1964).
The same loci in behavioral space can be used to describe the m a p
which is projected onto the striate cortex: Visual Area I or Area 17.
Again, there are two mirror components, one in each half of the brain.
There is a strong trend in the striate cortex maps to magnification of the
central region. I n the cat, the middle portion of the field has a cortical
territory m a n y times greater in proportion to t h a t which is given to
the more peripheral parts of the field (TALBOTand MARSttALL,1941).
I n primates, half of the cortical visual area is devoted to the central 10 ~
or so of the visual field, and the distant peripheral monocular fields are
scarcely represented at all (Fig. 4). This central magnification has been
found to parallel closely the greatly increased acuity which primates
show in the direction of the fovea (DANIEL and WmTTE~IDG]~, 1961;
COW~Y, 1964).
24
~sychol. ~orsch., Bd. 31
310
C.B. TREVAI~Tt{EN:
I n the primates, as in other mammals, there are several topographic
maps of visual space on the visual cortex. The different cortical areas
recei~ng map-like visual projections are partly innervated b y corticocortical links stemming from Area 17, and partly b y way of separate
parallel projections from subcortical structures. The striate map in the
monkey is reflected under a strip corresponding to the vertical meridian
onto the prestriate cortex (Areas 18 and 19). The dorsal part of the half
visual field represented in each hemisphere (i.e., the part corresponding
ARCUATE
GYRUS
(FRONTAL EYE
FIELD)
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CIRCUMSTRIATE BELT
CORTEX
.H /
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/~
45~ V E N T R A L
RIATE
CORTEX
CORTEX
INFERO TEMPORAL CORTEX
Fig. 4. Visual regions of the left cerebral cortex of a
monkey.See text.
H direction
of horizontal meridian in the right half of the visual field. V The vertical meridial
band (heavy cross-hatching) is connected to the corresponding region in the right
hemisphere over the splenium of the corpus callosum. Based on TALBOT and
M_~I~Stt~L (1961), DA~II~Land WttITTERIDGE(1961), NY]~t~S(1962), KIIYP=gSetal.
(1965)
to the ventral quadrant of the contralateral visual field) is mirrored
on the dorsal surface, and the ventral part (dorsal quadrant of the
visual field) is mirrored in the same way on the undersurface of the
occipital lobe (CowEu 1964; W~I~T~,RIDGE, 1965). As in the case of the
rectum, a map of eye movement m a y be obtained b y stimulation of these
topographically organized cortical areas (WAG~AN, 1964). A further
topography is found on the arcuate gyrus, the frontal eye field from
which eye movements m a y be obtained by stimulation (WAG~A~, 1964).
Both anatomical and electrophysiologieal studies indicate t h a t all
the systems in this complex array are topographically organized throughout every stage in the projection from the retinal surface to the cortex.
Thus, a substantial component of the cortical visual system represents a
laterally dispersed set of topographic maps of an anterior field within
the body-centered visual space - - the same space as t h a t found to be
Two Mechanisms of Vision in Primates
311
mapped onto the midbrain roof of all vertebrates. Moreover, the cortical
and collicular maps are strongly interconnected in a point-to-point
manner. SPnAGV~ (1966) has shown t h a t the striate areas and eolliculi
in the cat are coupled functionally in the control of visually-oriented
responses. There are indications t h a t a tangential order of relations across
the cortex is equivalent to a surface-towards-depths order of relations
among the tectal layers (Kvyps,~s, 1962).
The visual space around the body is thus represented in m a n y maps
in the brain, but always with respect to the axis of s y m m e t r y of the body
and its cffeetor apparatus. Each m a p is both representative of a visual
sensory field and integrated with the motor system. The repeated remapping of body-centered space does not mean t h a t the different cortical
and midbrain visual projections serve merely to reiterate the same
space-controlling motor functions. I t is clear that, while the tectal maps
represent the whole retina fairly uniformly, the map on Area 17 is disproportionally concerned with visual events near the line of regard and,
thus, with stimulation of the fovea. The extent of the cortical map
corresponds approximately with the territory within which visual fixation is deployed b y oeulomotor saccades.
Topographic Projections versus Neural Analyzer Systems
I believe it is necessary at this point to emphasize t h a t the topographic organization of these neural maps of behavioral space is an
intrinsic functional attribute of the visual system. This concept has
recently been rejected on the grounds that, when topographic displays
are disrupted or destroyed, perception of form remains intact (e. g.,
SrE~nu 1952; DOTY, 1961; Gibson, 1966). I t has been concluded t h a t
topographic order is primarily a morphogenetic device for assembling
the nervous system by growth so t h a t proper connections are made
between nerve cells. A number of procedures show t h a t the striate cortex
is not the field in which perceptual attributes of form, color, size,
luminance, texture, etc. are integrated. However, it is not necessary
t h a t the interactions b y which patterns of activity are evaluated with
respect to topographic neighborhoods be carried out at the level of a
collieular or cortical image because the whole projection system is specified in the same orderly arrangement. The dendritic fields deeper in the
brain, which are in synaptic relationship to these visual maps, are
probably structured in relation to this same general scheme. The topography is essentially a general principle of nerve system design which
provides a formal substrate for the control of motor functions in the
behavioral space. I t bears direct morphological and functional relationship to the organization of the motor system.
24*
312
C . B . TI~EVARTHEN :
Nevertheless, a system defining loci within the visual field relative to the body is only part of the mechanism of vision. Topographic
mapping of points in visual space onto points in motor space is not
sufficient to account for visual perception. Perceived space must be
structured by distinctions between loci and their surroundings, and such
distinctions require interaction between excitations of receptor cells.
Ideally, the neural elaboration of analyzers requires an organization of
connections which cuts across the topographies and goes beyond them,
so that, at any point in the topography, many features may be detected,
and each feature may be detected throughout the map.
Neural analyzers have been described for the cat and monkey visual
cortex which would be adequate for at least rudimentary resolution of
details of area and contour within patterns of luminance or hue on the
retina (D~VALols, 1966). Little is known about the kind of analyzers
adapted to vision of the image changes produced in orientation or locomotion. Presumably, velocity detectors or comparators of velocities
would be necessary for space determination by motion parallax. Furthermore, the sensitivities of peripheral vision or seotopic vision to relative
size, luminance, expansion of textures, etc. would require appropriate
analyzers. These would not necessarily have high resolution for local
features, but would require high sensitivity by summation of receptor
activities. Such analyzers have been described in lower organisms, in
particular in the retina and optic rectum of frogs and fish (see the contribution to this symposium by I~GL~). Velocity detectors have been
described in the retina of the rabbit where they are oriented in relation to
the normal position of the retina in behavioral space and to vestibular
canals and oculomotor muscles.
I t is probable that the functions of ambient and focal vision in
primates are served by two distinct populations of neural analyzers.
Furthermore, the receptor units of the primate collieuli are likely to be
appropriate for the resolutions made in ambient vision (cf. Hv~iP~g~u
and W~IS~A~Tz, 1967).
Visuo-motor Mechanisms in Primates Shown by the E//ects o/Selective
Lesions
Cortical and midbrain visual mechanisms stand in different relationship to the motor apparatus, and lesions made in midbrain or forebrain
of primates lead to dissociations of visuo-motor functions. The disturbances produced may be compared and contrasted with those described
by SchnEIDer, in this symposium, for the hamster.
The effects of removing the superior collienli in primates are complex
because these organs are part of an extensive system of interacting
Two Mechanisms of Vision in Primates
313
components, and, thus, differing tests have produced discordant conclusions; but some studies have emphasized the importance of the eollicull as midbrain sensory-motor integrating mechanisms providing a
visuo-spatial frame for action centered on the body as a whole.
When eolliculus lesions penetrate to deep layers of the tectum,
effects in cat and monkey are marked (BLAJ~, 1959; DE~xu162
1962; SP~AGu~, and MEIKL~, 1965). I n general, visual exploration and
orientation are greatly impaired. I n the cat, unilateral removM of one
superior eolliculus leads to neglect of events in the contralateral visual
field and heightened orientation to the ipsilateral half of space. There is
an initiM loss of spontaneous conjugate deviations of the eyes to the
eontralateral side (SP:aAGVE and Mv,IgL~., 1965). I n the monkey, there
are similar defects: a unilateral loss of optokinetie nystagmns when a
field of stripes is moved across from the side opposite the lesion, and
deficiency in visual fixation towards this same side. A m o n k e y w i t h b o t h
eollieuli completely removed stares fixedly into space, showing no
orientations to visual events though the projection to the cortex is
intact (DE~NY-B~ow~, 1962).
From stimulation studies, tIEss, B[rRGI and B~cg~R (1946) concluded
that, in the cat, connections from the visual eollieuli towards the motor
system of eyes, neck and anterior part of the trunk were the p a t h w a y of
"visual grasp reflexes."
The available information supports the view t h a t in primates, as in
simpler forms, the midbrain constitutes a mechanism capable of organizing general orienting movements of eyes, head and trunk within the
visual fields and controlling associated patterns of contraction in the
proximal musculature of the limbs. Apparently, there have been no
tests made of pattern discrimination independent of orientation in
collieuleetomized monkeys.
R e m o v a l of the cortical visual area (striate cortex, Area 17) in the
m o n k e y produces profound visual loss. KLgrV~ (1942) claimed t h a t
this operation left a monkey able to perform visual discriminations only
on the basis of total luminous flux received by the retina and concluded
t h a t visual space lost all differentiation after the operation. However,
D~u
and CHAmBerS (1955) found localization of small highcontrast moving targets to persist. Recently, W~ISK~ANTZ (1963) and
HUMPHREY and W~ISK~ANTZ (1967) have confirmed that, when properly
tested, monkeys with the striate cortex removed m a y reach accurately
for objects on visual cues and make a number of discriminations among
visual stimuli. They are insensitive to immobile stimuli but immediately
responsive to small moving or fluctuating light patterns. They are able
to discriminate on the basis of the degree to which white and black
314
C.B. TREVA~THEN:
areas are divided, i.e., to some feature related to the length of the whiteblack contour. Their spatial location of small oscillating or rotating objects may be remarkably accurate. They behave as if they have vision
of poor acuity but highly sensitive to motion and brightness, like vision
normally associated with the peripheral field or scotopic ilhlmination.
Normal visual perception in cat, monkey or man requires that a large
area of the cortex outside Area 17 remain intact. I n the monkey, deficits
of visual perception and of visuo-motor integration are produced b y
lesions in posterior-parietal cortex (Areas 18 and 19), but loss of this
region is not as catastrophic as predicted b y classical views (LAsHLEY,
1948; MISHKIg, 1966). Apparently, the functions lost b y removal of
extensive areas of prestriate cortex are readily compensated for. Complete lesions are difficult to achieve but m a y have more serious effects.
The deficits in response to visual patterns following parietal lesions in
the monkey are accompanied b y misreaching to small, stationary objects
(DEN?cY-Bxow~, 1962). The prestriate cortex appears to have a central
role in regulating visuo-spatial adjustments; and, as was mentioned
earlier, stimulation in this area produces an orderly pattern of conjugate
movements of the eyes related to the topographic projection in this
area (W'AGMA~, 1964; PASlK and PASlK, 1964a).
Complex visual deficits follow in the monkey with removal of tissue
from the infero-temporal cortex, which receives massive projection of
fibers from Area 19 (KtrYPE~s et al., 1965). This r e , o n is not known to
be organized topographically (Fig. 4). Bilateral ablation of the inferotemporal area produces defects in visual discrimination learning or
retention, which are most apparent if the lesions are made posteriorly
on each side in a region adjacent to the reveal field of Area 17 and at
the junction of the dorsal and ventral arms of Areas 18 and 19 (MisnKI~,
i966). This is when, the lesion is in a region adjacent to the cortex to
which any visual stimulus attended to would be transported as a result
of an oculomotor rotation to fixate it (Fig. 4). There is no associated
field defect or loss in visual acuity (CowEu and WmsK~a~Tz, 1967).
The loss is specifically related to vision of patterned effects, such as
two-dimensional figures, and monkeys with bilateral infero-temporal
lesions are inattentive to redundant stimulus features to which normal
monkeys are immediately responsive (1VhsHm?r and PI~I?alCAM, 1954;
WILSON and MISH~N, 1959; BUTT~, MIS~KIN and I~OSVOLD, 1965;
B V T T ~ and G ~ o ~ s x I , 1966). MIsHF~I~ has shown t h a t the infero-tempetal areas differ from the strictly mirror-symmetric topographic fields.
If one occipital lobe and the opposite infero-temporM area are removed,
the effects are minimal, but if the splenium of the corpus callosum is
then sectioned, fibers eonecting the :intact striate cortex with the intact
infero-temporal cortex in the other hemisphere are divided, and a severe
Two Mechanisms of Vision in Primates
315
deficit appears (MIsHKI~, 1966). Thus, the corpus cMlosum, in addition
to joining the topographic fields along the vertical meridian, is concerned
with pathways which pass from striate to prestriate, then across to the
other hemisphere and so to the opposite infero-temporal area. In consequence of these links, each infero-temporal cortex may function in
association with the topographic fields of both hemispheres and may be
oriented to either half of the behavioral space.
The laterM-frontal region of the cortex is connected with the inferotemporal cortex in both directions ( K u u
et al., 1965). In monkeys,
frontal lesions produce no defect in visual discrimination, but cause specific loss in a delayed response task (JAcobseN, 1935; JACO}3SEN,
WOLF and JACKSON, 1935; MISHKIN and P ~ I ~ A ~ , 1955, 1956; PI~IB~A~
and M~SHK~N, 1956) and indifference to the consequences (reinforcement)
of responses (PmB~AM, 1960). In the delayed response test, a monkey is
required to respond to an object with no present visual distinctiveness,
but on the basis of something seen a short time before in close spatial
relation to it. Adjacent to this lateral-frontal area is the frontal eye field
from which conjugate deviations of the eyes are obtained on stimulation
(WA~A~, 1964). An apparently topographically organized projection
from prestriate areas to the arcuate gyms brings this area into relation
with the posterior visuo-spatial mechanism. A lesion at the apex of the
areuate gyrus leads to neglect of the opposite half of space, possibly by
interrupting fibers from the prestriate cortex (W~LcH and ST~T~VILL~, 1958).
In man, damage to the striate cortex or the projection to it results
in losses of vision in parts of the visual field which are centered appropriately in the topography but are generally not as extensive as would be
predicted from the extent of the lesion in relation to the topography of
the retino-striate projection (T~gB~l~, BATTE~SBY and B~DE]r 1960).
This is also the case in the monkey (CowwY and W~ISK~A~Z, 1967).
Losses of tissue from the prestriate cortex, when restricted to one side,
may produce unilateral neglect of figures on the contralaterM side
(AJv~IAGUEn~ and tt~CA~N, 1960). This is associated with a corresponding deficit of exploratory eye movements (Lu~I~, 1966). Bilateral
occipito-parietal lesions may result in disturbances in the perception of
complex or confused visual figures without visual field defect (LlssAvn~,
1890). In Balint's syndrome, for example, the number of objects which
may be perceived simultaneously is reduced to one (H~c~E~ and AZu~I~GUE~I~, 1954; LUCIA, 1959). If two objects are present, one disappears
while the other is inspected. This syndrome is also associated with a
defect in relocating gaze (Lv~I~, 1966).
Great is the variety of distinct losses of perceptual synthesis or
agnosias which have been found to occur following lesions in the exten-
316
C.B. T a ~ v A ~ :
sive parietal cortex of man. The most characteristic visuo-psychic
defect is a disturbance of the synthesis of perceptual signs into a perceived
object or figure, called "Amorphosynthesis" by D ~ s Y - B ~ o w ~ etal.
(1952). We should especially note that this defect is invariably accompanied by abnormal exploratory eye movement, i.e., of spontaneous
or intelligent shifts of regard. Drawings often contain automatic reiterations of simple figures representing the patient's attempts to overcome
his inability to make order of the configuration presented to him.
Frontal lesions in man disturb oculomotor activities and cause
compulsive attention to present stimuli and a lack of initiative for
complex acts (AJuRIAGUE~RAand HAcA~r 1960; LucIA, 1966). The
description of a frontal patient by LunIA ei al. (1966) shows an inability
to move the eye away from immediately compelling features of a scene
and, thus, an inability to make the appropriate selection of inspections
to solve a specific perceptual task.
An Hypothesis o] Visuo-motor Functions in Primates
The visual and motor deficits produced by cortical lesions in man
and monkeys allow a tentative formulation of forebrain visual functions
in primates.
The spatial frame for orientation of reaching movements is partly
established by ambient vision which also regulates the orientation of
the body as a whole and general locomotion. For the reafferent visual
functions upon which these movements depend, the midbrain tectum is
essential. I t remains to be determined, however, to what extent cortex
and rectum overlap in their regulation of behavior within the ambient
visual field in primates.
In the cerebral cortex, a posterior visual system organizes the
samples of information taken by focal vision during successive fixations
within a global matrix of wide spatial extent. There is a process of
"trading off" local, detailed vision against a wide-spread, less discriminating vision (BoY~TO~, 1960). In free behavior, selective eye movements
regulated by an occipito-parietal cortical system perform this. The
process determining each selective movement is centripetal, because the
destination or target of an eye movement is partly determined by
distinctions resolved at a locus some distance from the fovea in the parafoveal field. The construction of a fairly complete model of a portion of
physical reality thus appears to require constant reciprocal interchange
between peripheral spatial apprehension and foveal resolution of configuration, hue, reflection and shadow patterns, etc. The fine foveM
resolution found in primates is related to the greatly magnified foveM
region of Area 17 which is in dh~ect communication with a massive
neuronal mechanism in the adjacent infero-temporal cortex. Ablation
Two Mechanisms of Vision in Primates
317
experiments show t h a t this latter area is of decisive importance to the
recognition and learning of complex patterns.
An anterior forebrain visual mechanism, represented by the frontal
eye fields and the adjacent lateral fro:~tal cortex, m a y be highly concerned with the relationships between behavioral schemata (in the sense
of H e a d or Bartlett) and visual explorations and fixations. When a
monkey solves a spatial task, like a delayed response test, or a test which
requires him to bring together two boxes and stack t h e m to reach a
suspended banana, his gaze must frequently be directed to remembered
and expected, but not seen, features. The same is true when he is looking
for an object, although such looking m a y be anything but systematic.
The shift of gaze in solving a spatial riddle or searching out a hypothesized relationship m a y be called centriJugal in contrast to the visuomotor activity previously called centripetal. With frontal lesions there
is a loss of this kind of visual sampling and hence of the ability to adapt
to spatial alterations or to extensive temporo-spatial relationships.
This s u m m a r y emphasizes the importance of visuo-motor, especially
visuo-oculomotor regulations in the normal course of visual perception.
The eye movements under cortical control allow distribution of focal
vision within a portion of space to which the organism as a whole is
oriented. Coordination of refined manipulatory activity with focal vision
is also dependent upon cortical processes. The evidence from lesion
studies is t h a t both visuo-oeulomotor and visuo-manual coordination
is obtained b y multiple corticofugal projections and convergence within
brainstem and spinal motor systems where integration of motor with
visual perceptual processes occurs ( M u
SPEn~Y and McCv~mr, 1962 ;
PasIK and PaSlK, 1964a).
Experiments with Split-brain Monkeys
We now return to the experiments with monkeys which were mentioned in the introduction to this paper. The split-brain preparation
offers one way, albeit indirect, of obser~ng the distribution of visuM
functions in the brain, and of bringing out anatomically based dissociations of these functions.
The experiments to be described here were performed with surgical
bisection of the forebrain and division of the optic chiasma so that, as
far as the forebrain system is concerned, the two mirror halves of the
visuo-spatial projection to the forebrain were each receiving input from
only one eye (the ipsilateral one), and all direct interhemispheric
communication was broken.
Cutting the chiasma abolishes binocular stereopsis (TI~EVA~TIIE~,
unpublished) and eliminates the early warning system of the temporal
318
C.B. TREVARTHEN:
monocular crescent of the visual field. Thus, immediately after surgery,
split-brain animals make errors of depth estimation and are disconcerted
b y things coming on them from behind. Nevertheless, they look perfectly
alert and normal. They can converge the eyes normally and move with
perfect synchrony and efficiency. Though a few distance errors are made
initially, reaching and manipulation of objects is performed with high
accuracy with either hand, and the two hands are used collaboratively.
There are, nevertheless, some most interesting discoordinations of
voluntary use of the hands which I shall describe.
/\
POLARIZERS
PROJECTED
STIMULUS
Fig. 5. The apparatus for testing vision of split-brain monkeys
I n the visual descrimination experiments discussed below, the
monkey is oriented and seated; he places his head voluntarily into a fixed
position behind a mask which serves approximately like a bite-board
(Fig. 5). He is required to look at and choose by hand between two small
visual stimuli projected on translucent screens straight in front of him
and separated horizontally b y 20 ~. If he pushes one of the two stimuli,
a peanut is dropped in front of him. If he pushes the other stimulus, both
stimuli disappear, and he gets no reward. I n half the trials, the correct
stimulus appears on the right side ; in the other half, it is on the left side.
By polarizing the stimuli and putting orthogonally oriented polarizing filters in front of the eye-holes of the mask, it is possible to project
stimuli visible to only one eye or the other; thus, different overlapping
stimuli can be projected simultaneously but separately to the two eyes
(see Fig. 7). This technique enables study of double learning with conflieting stimuli and other studies of the interaction of visuo-motor functions in the two separated cerebral hemispheres (T~]~VA~TI~]~N,1962a, b,
1965).
319
Two Mechanisms of Vision in Primates
Two-Mirror Orienting Systems (TR]~V~a~Tr[~N, 1965, pp. 103--106)
I n this experiment, evidence was obtained that each cortical hemisphere is concerned with oculomotor and perceptual orientation to
only one half of the focal visual field in behavioral space. A monkey
was operated upon after learning to push a 2 ~ black triangle and not an
equal area black square (Fig. 6). Three days after midline division of the
corpus callosum, anterior and hippocampal eommissures, and of the
optic chiasma, this monkey scored almost perfectly as long as both eyes
were open. But when the stimuli were projected unpredictably to one
[
RIGHT EYE
~
'
I
I
LEFT
CENTER
RIGHT
i
Fig. 6. The stimuli seen by a monkey with chiasma and corpus callosum divided
as his gaze shifts from the left stimulus, to the center and to the right stimulus
eye at a time, the other eye being free to see everything but the stimuli,
the score dropped to chance. The monkey always ignored the stimulus
on the same side as the eye to which the two stimuli were projected. He
neglected the ipsilateral half of the task.
After about 100 trials with each eye, the monocular choices became
correct. He had learned to decide what to do with only one stimulus
visible, or else he had learned to look over to the hemianopic side with
each eye so as to catch the other stimulus. This experiment suggests
that when a chiasm-eallosum sectioned monkey looks at an object with
the left eye, he may not think to look for something a few degrees to the
left side of the object before making a manual response, unless he has
been trained to do so. With the right eye he neglects the things to the
right of where he is looking. While both eyes are open, left-ward and
right-ward reorientation of the eyes are made so both stimuli are
responded to, the two forebrains sharing direction of responses in spite
of their separation. This suggests, in turn, that while both eyes were
seeing, the two cerebral hemispheres were coordinated by virtue of
their coupling through the mechanisms of brain stem and cord. When
320
C.B.T~EvA~T~EN:
the stimuli were projected to only one eye, an orientational set favoring
one half of space was produced. Defects in oculomotor orientation
(recentering) of split-brain monkeys have been recorded during optokinetic nystagmus b y PaSIK and PASIK (1964b).
Mirror Prehensile Systems (DowNEI% 1959; TtgEVAtCTIIEN, 1962a, b;
GAZZ~NmA, 1964)
I n addition to the orientation effects demonstrated in the preceding
experiment, split-brain monkeys tested in the above apparatus always
show spontaneous preference for working with a particular hand when
vision is restricted to one eye. With the left eye, the right hand is chosen.
If the stimuli are presented consistently to the right eye, there is a
switchover to the left hand. If, after settling into these preferred pairings,
a split-brain subject is forced to work with right eye and right hand or
left eye and left hand, these ipsilaterM pairs are at first badly discoordinated. There are characteristic disorders of responses to the stimuli.
Sometimes, the reaching movement does not come as soon as the stimulus
is looked at; movements of the limb are usually impulsive and rather
clumsy with poor positioning of the fingers. We find, for example, no
neatly timed pointing at the target with an extended index finger. The
choices made between two stimuli are also very erratic; for a run of
!0 to 20 trials, the responses m a y be correct, then in the next group,
the score drops to chance. Occasionally, a deliberately aimed push is
made to one side of the two stimulus panels, as if the monkey had halucinated a stimulus at a point where none was presented. This m a y reflect
a disorder of proprioceptive preparation for the movement and thus in
its projection into the space around the body.
After a time, ipsilateral eye-hand pairs m a y be as well-coordinated
as the contralateral ones, but the post-operative deficits indicate t h a t
there is a functional mirror grouping of left hand movement control with
the visual apparatus concerned with the left half of visual space. Taking
into account the results of the preceding experiment, we conclude t h a t
each half of the cerebrum is concerned primarily with the opposite side
of a bisymmetric oculomotor and manual space in front of the monkey.
With left eye and left hand, or right eye and right hand, a split-brain
monkey with chiasma sectioned cannot easily guide his hand to where
he is looking, nor look to where he intends to reach to see if it is a correctly
chosen place.
Further Motor Functions in Split-Brain Monkeys
l~ecently I have been measuring the ability of split-brain baboons to
perform a complex manual task with vision of the task kept to one cortex
(Tn~vA~T~N, 1968). The testing was done with a small problem box
Two ~eehanisms of Vision in Primates
321
placed straight in front of the subject who worked behind a mask in
fixed orientation as in the visual discrimination tests. The orientation
of the box was switched from trial to trial, unpredictably, to make the
task spatially balanced.
As long as the hand performing has been trained to do all the steps
in the task, and if it is contralateral to the eye with is uncovered, performance is generally normal. With the contrMateral eye covered, the
monkey for a few trials is at first wooden and rather clumsy, and movements of this same hand are clumsy and clearly more dependent on
reactions to touch and other non-visual guidance. With either hand,
errors m a y occur because of unilateral neglect - - the monkey sometimes
sees and thinks of only half of the task in front of him and often makes a
confident move to the wrong half in the visible field, not apprehending
some visual orientation cue in the other half field.
Particularly interesting effects occur when a preoperatively learned
habit to open the box has been one involving collaborative use of the
two hands. After the forebrain is split, restriction of activity to one hand
may result in bizarre holes in the skill or strategy. Steps normally performed by the other hand are totally neglected for many trials until a
new strategy is worked out. Here, vision with either one or both eyes may
not help. The trouble is that the one half-brain in action does not know
that the other hand cannot come to do its job. A new way of looking at
the task must be worked out to overcome this lack. Unlike a normal
monkey, the split-brain monkey cannot think of this easily, and he goes
on repeatedly omitting the step or waiting for it to be performed and
then giving up. Elsewhere I have suggested that the cortical lateralization of strategies for manipulative skill m a y m a y offer an elementary
model of the attainment of a cerebral asymmetry of cognitive control in
man (TI%EVAI~TIIEIg, 1968).
Sometimes, non-communication between the cortices produces redundant manual responses -- responses to an object ~dll be simultaneously
performed by two hands at once so that they collide. When stimuli are
presented to both eyes simultaneously, both hands may respond redundantly, either to one midline point if the stimuli are coincident, or
symmetrically to two points spaced at equal distances a little to the
side. A free split-brain monkey will reach to one peanut with both hands,
or simultaneously to two peanuts falling either side of him at one moment.
Convergent responses of the two hands to one object may even lead to
brief episodes of intermanual conflict and a tug-of-war, or a game of tag
between the hands.
These observations support the conclusion that separating the cerebral cortices m a y separate two distinct systems which can organize
vohintary activity of the hands. Similar effects were reported by
322
C.B. TREV~RT~N:
K]~D
and WATTS (1934) for callosum sectioned monkeys, and dissociation of voluntary manuM responses is seen in "split-brain" human
patients (Ax~LAITIS, 1944; GAZZA~mA, B O G ~ and S P ~ Y , 1962).
Such transitory conflicts of spontaneous motor activity are not reported
for other motor organs. In general, there are many avenues of reafferent
control which regulate the coordinated activity of the two sides of the
body or of the limbs in split-brain individuals. I t is interesting that,
when the split-brain baboon looks down at his conflicting hands, the
tug-of-war immediately stops. The discordant sets for eontroi of motor
activity of the limbs are brought into harmony when vision is obtained
of both hands.
In contrast to the mirror oculomotor or visuo-manual effects and
dissociations of voluntary use of the hands in the field of focal vision, no
abnormalities are seen in locomotion. The hands are important locomotor organs in monkeys. Split-brain rhesus monkeys or baboons climb
with agility and speed as soon as they recover from surgery and the
anesthetic. Here the visual frame for action is entirely unified, and we see
proper rhythmic coordination of proximal muscles and trunk together
with accurately timed adjustments of the hands for grasping or pushing,
regardless where the gaze is directed. The dissociation in use of the hands
is specific for prehension and manipulation of small objects.
The observations of visuo-motor integrations in split-brain monkeys
show that as long as somatosensory or proprioceptive pathways of
reafferent control are insufficiently active, there may be dissociation of
movements controlled by focal vision in left and right halves of behavioral space, but the mechanisms of ambient vision show no such dissociation.
This conclusion receives further support from the results of visual
discrimination tests.
Double Vision Tests. Dissociation el Mechanisms o/Visual Perception
( T ~ v ~ T ~ E N , 1962 b)
Subjects with optic chiasma and interhemispheric commissures
sectioned show that each eye-hemisphere system learns separately to
distinguish patterned visual stimuli when they are trained to respond in
a Yerkes type locomotor choice apparatus (cat) or else with the forelimbs
alone (cat and monkey). There are many experiments confirming the
"split-brMn" or "two-learning-systems" effect, from the classic studies
of MYnas (1956, 1961) with the cat, through experiments with the
monkey (SPEn~u 1961), to the recent tests made by GAzzA~mn, B o G ~
and SPn~Y (1962, 1965) with human cases subjected to cMlosum section
to prevent interhemispheric spread of epilepsy. Each cerebral hemisphere
Two Mechanisms of Vision in Primates
323
is a separate perceptive and cognitive system and learns separately when
the commissural cross-connections between the two cerebral cortices
are cut.
However, experiments with the cat show t h a t a range of visuo-motor
integrations is performed b y the midbrain visual system, especially
when simple luminous differences or flashing light stimuli are used
(M~IKL]~ and S~c~z]~, 1960; 1VIEIKLE, 1964; VO~IDA, 1963; FlSCHMAN
and Mv.It~LE, 1965) and when less focalized or instrumentally-controlled
responses are called for (Vo~cEIDA, 1963; SPnAOUE and MEIXLE,1965).
In the monkey, the two halves of the cerebral visual mechanism
appear to be totally independent in control of simple manual responses
following split-brain surgery as long as successive monocular training
and retention tests are used (DowNE~, 1958; SPERRY, ]958). No
evidence of interactions for pattern or for color or luminosity discriminations has been obtained with successive testing (HA~ILTO~r and
GAZZA~IOA, 1964). However, I have found t h a t when certain conflicting
stimuli are given simultaneously with the polarized stimulus technique
(Fig. 7), there m a y be an interaction producing suppression of vision
in one half of the brain during binocular training, and this shows up
in subsequent monocular retention tests (T~EvA~T~r~, 1962b, 1965).
The conclusions from m y experiments are as follows. A split-brain
monkey can see a cross with one half-brain while seeing a circle with
the other half-brain - - and reach with one hand to choose these two
incompatible patterns without confusion. W h a t he is oriented to visually
can be both a + and a 0 at the same time. The identities are kept apart
in the brain, and either or both can be taken as the goal of the manual
response.
However, the object (panel) responded to cannot immediately be
seen as simultaneously dark and light or blue and red in the two brain
halves. When horizontally aligned pairs of these stimuli are given overlapping in opposite orientation to the two halves of the brain (one to
each half as in Fig. 7), one alternative view is suppressed. When the two
eyes and half brains are tested separately for retention after binocular
training, both halves respond the same way to one of the stimuli, in
spite of the fact t h a t one eye has never " s e e n " this stimulus as correct
during the binocular training, except by some internal perceptual transfer
from the attending half-brain against the current input of conflicting
information from the unattended eye. Presumably, vision of the stimuli
had been internally suppressed for the second eye as long as the first eye
was in use.
I t is possible that two different kinds of vision were employed for
the patterned stimuli on the one hand, and for the brightness or color
differences on the other. Certain kinds of patterned stimuli seemed to
324
C.B. TREVAtCTHEN:
lie between these extremes; for example, the pair "5-pointed star versus
6-pointed s t a r " showed an intermediate degree of interaction in the
double learning test. I suggest t h a t the interactions resulted from
intrusion of tectal visual processes analyzing the stimuli according to
certain space-defining attributes. The "cross" and the "circle" were
recognized b y cortical mechanisms of focal vision alone.
(
POLA.IZER
ON RIGHT EYE
/
/ /
POLAR,ZER
ON L E F T EYE
FIELD
LEFT
EY~,~N
RIGHT
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'[
STIMULI SEEN
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STIMULI
Iklll[ IIIllll
,
~--2o~
\
/
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Fig. 7. The projection of the visual stimuli in tests of the split-brain monkey,
See text
Interocular Comparisons (T~vAnTEw~, 1963, 1965, and Discussion on
pp. 144--147 in the Latter Publication)
Tests demanding comparison of stimuli m a y be used to demonstrate
interocular communication directly. Using polarizing filters again for
separate stimulation of the eyes, I have tested for the ability of a monkey
with chiasma and forebrain commissures sectioned, to choose the larger
of two thin black annuli of different diameters projected onto a white
screen, one stimulus of the pair being presented to each half of the brain
(Fig. 8). A tendency to respond to the absolute size of one or the other
of the stimuli was overcome, and the split-brain monkey, after extensive
Two Mechanisms of Vision in Primates
325
practice, made a j u d g m e n t of relative size with little hesitation for each
of the 8 pairs of adjacent circle sizes. To help the m o n k e y over his
reciprocal half-field deficits, the left stimulus was projected to the right
eye and vice-versa. So, if he looked between the stimuli, both stimuli
would be received b y the brain and seen on either side of the vertical
meridian straight in front of the head (see Figs. 6 and 7).
0
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Fig. 8. The test for interoeular comparison of size of circles. The stimulus pairs are
shown as presented on the response panels. Each pair was presented equally often in
each of the two possible orientations. A Pre-surgieal training; B Post surgical performance with voluntary choice of the right hand (some redundant left handed
responses occurred). Both stimuli visible to each eye; C Performance with alternated
groups of 32 trials performed by left and right hands. Both stimuli visible to each
eye; D Performance as in C but with the stimuli projected separately; left stimulus
to right eye, right stimulus to left eye
A particular m e t h o d was used to overcome the m o n k e y ' s ability to
recognize the absolute sizes of the projected circles and to play his
chances to win. I t has been suggested t h a t in this experiment the m o n k e y
could attain a high score w i t h o u t using interocular comparison b y
employing a s t r a t e g y of this kind (LEE-TE~o and S P ] ~ u 1966). I n the
full test, five different circles were used, and in each trial an adjacent
pair of circles in the series was presented. Since the largest of each pair
was presented on the left and on the right in different trials, this makes a
25
s
Forsch., Bd. 31
326
C.B. TREVA!~THE~:
total of eight different pairs of circles. The pairs were presented in a
pseudo-random sequence, balanced so t h a t the proportions of change
in size, and of reversal of size, were rewarded equally. Thus, the monkey
could not make inferences on the basis of the order of occurrence of the
stimuli. I n each run of 32 consecutive trials, there were four occurrences
of each of the eight pairs of circles. The testing was continued until a
criterion of p =-0.01 was achieved for each of the eight pairs simultaneously in a block of 64 consecutive trials. To cheat, the monkey could
employ unilateral rules such as "always respond to the largest size no
matter which side it appears; never respond to the smallest." Using
both of these rules together perfectly, he could not obtain more than
75 percent correct responses. Alternatively, he could adopt a successive
search - - "look first for the largest (Number 1) either side, then the next
largest (Number 2) either side, etc." B u t it is inconceivable that even a
normal h u m a n subject could perform this task on absolute size recognition this way and give the calm, unhesitating and short-latency responses
which were observed. When tested with equal size circles presented, or
with circles presented to one eye only, the performance immediately
became hesitant, and the score dropped to chance. The same occurred
if one eye was covered and the stimuli were presented polarized, as in
the test for interocular comparison. Under these circumstances the controls appear adequate, and I conclude that the circles were compared
interoeularly.
Choice between the circles based on their relative size had been
learned preoperatively. Presumably, cortical visual analyzers of curvature were still involved post-operatively, and, b y means of the vertical
links between forebrain and midbrain visual mechanisms, poorly defined
midbrain images carrying information about relative size were then
brought up to mark to allow comparison between them over the midline.
An orientation tendency integrated in the midbrMn visual mechanism is
presumed to have guided responses of eyes and hand toward the larger
stimulus.
I t is interesting in connection with this experiment that, though
we have very poor acuity for contours at the far periphery, it is possible
to make immediate and accurate orientations to left or right stimuli in
the monocular temporal crescents which have relatively poor cortical
representation. Also, differences in size, or brightness, or contour-fragmentation seem to be easily but fleetingly apprehended. I t is suggested
t h a t the mid-brain intercommunications m a y participate in these
primary visual effects which structure the wide frame for large motor
orientations and t h a t the same analyzers for space-sensitive features as
operate for the peripheral parts of the field also operate within the
central visual field where the paired circles were presented to the monkey.
Two Mechanisms of Vision in Primates
327
I t is possibly important to the success of this experiment that the
response required, though manual, was of a simple form involving no
more than a jab directed to the left or right panel.
Cortical Detectors. The Local Feature o/Contour Intersection
(T~]nVA~TH~,~, 1963)
Although a monkey with forebrain divided can learn to compare
circles of differing sizes when they are projected separately to the two
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Fig. 9. A further test for interhemispheric integration. The monkey was required
to choose the pattern, marked by an asterisk in each case, where the black bar was
at right angles to the striated backgrounds
halves of the visual system, a bilateral comparison of the orientation
of a black bar and a striped background is impossible (Fig. 9). A monkey
with chiasma and forebrain commissures divided could easily choose a
vertical bar against horizontal stripes, or a horizontal bar against vertical
stripes, and reject either of the two combinations with the bars parallel
to the stripes, as long as both bars and background were proiected to one
cortex. The two cortices learned this task separately and successively
with no signs of transfer between them. When bars and stripes were
projected to separated cortices, the score remained at chance for 800 trials,
while within-cortex choices were perfect.
This and the preceding experiment help draw a boundary between
strictly cortical and cortico-sub-hemispheric visual processes. I n the
25*
328
C.B. TREVARTttEN:
present test, the intersection of the stripes by the bars within one and
the same cortical mechanism provides the criterion by which the visual
system discriminates between the rewarded and non-rewarded projection
panels.
Conclusions
The survey of anatomical and physiological features of the primate
brain, and the results of behavioral experiments following surgery to
parts of the visuo-motor mechanism lead to the conclusion t h a t two
kinds of visual function m a y be distinguished in the regulation of primate
behavior. One is ambient or extensive, the other is local or intensive.
I n primates, ambient vision resembles the vision of primitive active
vertebrates. Compared with focal vision, it has low angular resolution
for stationary features, low sensitivity to relative position, orientation,
luminance or hue, but high sensitivity to change in any of these attributes. These characteristics are little changed under scotopie conditions.
To some extent, there is even disinhibition of vision in the peripheral
field when the central photopic system is less active. This possibly suggests t h a t the rod mechanism of a duplex retina is organized to serve
ambient vision ; the distribution of rods in the retina is obviously appropriate. Nevertheless, under photopic conditions, a part of the cone
population contributes to ambient vision because the rod system is
quite insensitive at the photopic level.
At any instant, an extensive portion of the behavioral space around
the body is mapped b y this ambient visual mode ; in primates, somewhat
more than a frontal hemisphere is apprehended. With large rotations of
the head or whole body, an animal m a y quickly scan all of the space close
to his body and thus obtain a visual impression of the large features in it.
The visual mechanism is strongly stimulated by parallax changes caused
b y translation of the eye, and the receptor mechanism is particularly
sensitive to the velocities of displacement of discontinuities in the light
pattern on the retina. Velocity patterns thus largely provide the information of the three-dimensional visual space near the body. This
vision is, in a sense, " d r i v e n " by locomotion or turning the head in
space; angular velocities ranging from about 1~ per second to about
100 times this are measured and compared in this process. The visual
space thus apprehended is adequate for governing locomotion or postural
adjustments.
The characteristics of ambient vision have certain affinities and
relationships with other spatial sense modalities. Together, all the
modalities which detect events distant from the body over a wide field
help build a unified and stable space in three dimensions - - a context
for action and perception.
Two Mechanisms of Vision in Primates
329
Comparisons of the visual projections to the midbrain in various
vertebrates lead to the conclusion that, in primates, the primitive
midbrMn visual mechanism controlling orientation in space has been
augmented but not supereeded by the addition of topographically organized forebrain visual mechanisms. The two parts of the brain appear to
function in close association with one another and with other parts of the
central nervous system in the integration of a space frame, a process
which, in man, leaves scant indications in consciousness.
I n contrast with this vision of ambient space, focal vision, enormously developed in diurnal primates, is applied to obtain detailed vision.
A primate is capable of resolving detail of form subtending fractions of a
minute of are and is sensitive to the very slightest difference in position,
orientation, luminance or hue. At the fovea, the sensitivity of the focal
mode of vision to stimulus change or movement exceeds the sensitivity
at areas remote from the line of regard.
The spatial scope of focal vision is, at any instant, very restricted.
With sampling or scanning movements of the eyes, sharp, clear and
intense discrimination is extended from the one to two degrees subtended by the fovea to include a wide portion of the central field. For
inspection of very small territories, about 0.5 ~ or less, the eyes are fixated. The muscles of limbs, trunk and neck are maintained tonically
clamped so t h a t only minute displacements of the eyes are caused by
them, or else the head moves slowly, damped by high inertia, and the
motion is compensated for accurately by opposite rotations of the eyes.
Stabilization of the spatial frame frees focal vision so t h a t an area of
interest m a y be brought to full attention and analyzed as if carried close
in b y a zoom lens.
During intent fixation, there are small saccades, down to about
5 minutes of angle. Areas subtending up to 30 ~ are explored b y larger
oculomotor saccades. For territories larger than this, the head and
eyes move in concert, and the motions add to give a single saceadic displacement or a chain of saccades (SANDERS, 1963). When motion within
the visual world is obtained by movements of the trunk and limbs,
visual sampling b y discrete saccadic steps and "place-holding" compensatory drifts tends to give over partially or completely to transportations
of the eyes within the ambient visual frame.
During fixation, adaptation of focal vision to stimuli is prevented
by minute drifting movements of the eyes which displace the retinal
image at an average rate of six minutes of arc per second (YA~BUS, 1967).
Therefore, in keeping with the resolving power of this mode of vision,
the image movements which "drive" or activate focal vision are of the
order of 1/100 as fast as those which are optimal for "driving" ambient
vision extending over the whole field.
330
C.B. TREV~THEN:
The effects of brain lesions indicate that the sensory and motor
functions pertaining to focal vision are performed primarily within the
cerebral cortex. In the striate cortex, a high resolution analyzer system
centered around the reveal projection is massively represented. The
determination of fixation drifts separated by saccadic displacements
of the eyes is, I would conclude, essentially a cortical function. Likewise,
fine manipulative and other praxic activities are primarily regulated
there.
The split-brain experiments suggest two visual modes of function
which are differently represented in the cerebral cortex and in the
midbrain. When they are disconnected, the two forebrains of a monkey
form mirror systems for the control of oculomotor or manual orientations
aimed at the contralateral half of the space surrounding the body.
Perception-generating and manipulation-controlling schemata of high
resolution may be built up independently in the two surgically separated
hemispheres and so give rise to separate frames for fine, praxic action.
Under these conditions, interhemispherie conflict may lead to redundant
or antagonistic manual responses.
Surprisingly, eallosum-sectioning does not upset the locomotion and
posture of a cat, a monkey, or a man in any easily detected way. A
split-brain subject faces a point of interest in visual space as a single
oriented individual. Simple reaching with either hand to this point is
accurate. Locomotion to it, even climbing towards it in a three-dimensional structure of supports, is little changed. Brain stem integrations,
as well as sensory feedback from peripheral detection of the movements
of parts on both sides of the body, would appear to sustain a single
regulatory frame. The midbrain provides an important place of convergence in this centrencephalic system. Even in primates, the relatively
small midbrain rectum may serve in visual analysis, providing a visual
spatial frame in which the animal moves by detecting contours and
measuring brightness and color inequalities. Reorientations of the body
as a whole in a visual spatial frame are regulated in part by the older
visuo-motor centers of the brain stem, whereas local discriminatory
responses involving complicated recognition processes are exclusively
telencephalic.
Thus, the experiments with split-brain monkeys give support to the
theory of visual brain functions which was derived from considerations
of the functional anatomy of the vertebrate brain and of the close
relationship between visual perception and action.
Full visual perception requires apprehension of the features of objects
properly attributed to a spatial configuration and properly located with
Two Mechanisms of Vision in Primates
331
respect to the body. The distinction between ambient and focal vision
leaves open the question of how this perceptual synthesis is obtained. We
have space only for a very cursory discussion of the linking functions
here.
1. There are processes which lead automatically to segregation of
ambient and focal visual analysis. First among these are the complementary receptor ]unctions themselves. For example, sensory adaptation of
the low resolution, high gain peripheral visual receptor units leads to
rapid fading out of the lateral fields when the eye is held nearly stationary
in front of a stationary array, as in fixation, l~esolution in focal vision is
low when image motion stimulates the peripheral receptors strongly. When
light falls to scotopic levels, there is insufficient stimulation of the high
resolution photopic system which, conversely, is favored in high light.
2. A second form of interaction appears to involve reciprocal inhibitory coupling and to serve attentional shifts from one mode to the other.
If, under fixation, the peripheral field has faded from view, movement
of a peripheral element is highly visible, and it causes momentary
depression of central acuity, even if the eyes do not move off fixation.
Also, when several elements are present as noise simultaneously in the
visual field, only those which lie very near the fovea are resolved - tunnel vision is produced. The same degree of visual resolution is possible
far from the fovea when only one element is presented (M~cKWO~TH,
1965). The shifts in visual resolution which occur as one becomes adapted
to seotopie vision also indicate thet removal of stimulation from the
photopie system may unload or disinhibit the system served by the
rods. Such interactive effects are very numerous, and they undoubtedly
underlie some well-known laboratory perceptual effects.
3. The course of interaction also depends upon the di]]erential speeds
of the two systems. Oculomotor tracking responses to drift of the whole
or part of the field are known to occur with shorter latency than saecadic
responses aimed to catch a particular local feature (RASH~ASS, 1961).
Discharges of peripheral sensory systems often show both very short
latency and brief components as well as longer latency and more persistent components. B]~K]~Su who has demonstrated that the location of
stimuli depends upon temporal interactions precise to tenths of a millisecond, has concluded that the localizing signals are conducted into the
brain by short latency components, whereas the later parts of the
afferent discharge establish the intensity of stimulation (B]~K]~Su 1967).
In the visual systems of vertebrates, different components have widely
different conduction speeds so that an environmental event produces
a succession of sensory events. In primates, the geniculo-striate system
appears to have slow and fast components in which the neurones are of
different size. The former slow, small-celled component is primarily
332
C.B. TI~EVAI~THEN:
concerned with photopie vision and is largest for the central part of the
visual field; the latter with large cells is concerned with scotopie or rod
vision and represents the fields more uniformly (HAssL~, 1966). Furthermore, a precise topographic mapping of the visual projection onto the
striate cortex using small light flashes is obtained only for the short
latency component of the evoked response (DAnieL and W~ITT~IDGr,
1961). I t appears that each visual event first establishes spatial reference
within the ambient visual spatial frame in midbrain and cortex. Then
a process of analysis is initiated which is accompanied by an orientation
movement, bringing focal capacities fully to bear upen the stimulus.
4. The ocular orientation movements which shift the retinal image of a
peripheral point onto the fovea serve to link spatial location with resolution of identity (SA~D]~s, 1963). Motor acts of precisely defined spatial
and temporal extent estabhsh relationships between ambient and focal
vision. Some of these acts are effective by changing the paramaters of
stimulation to favor one or other visual mode. Thus, steady translation
of the eyes in locomotion gives the impression of a strong stimulation
of the peripheral field of global vision and depresses focal attention.
Fixation, accommodation and possibly pupillary constriction increase
the sharpness of the image, and hence the stimulation of the high acuity
system; at the same time, one experiences a fall in peripheral visual
attention.
5. Beyond the above essentially peripheral mechanisms, memory and
processes o/cognition are essential to perception of identities in space.
The ongoing perception of identities within appropriate contexts requires
more than moment by moment accounting of orientation within a bodycentered spatial field and statistical accumulation of excitation in
feature-detecting analyzers. Experience would be a disjointed succession
of attempts at adaptation unless there were formulated schemata or
plans for action linking representations in the brain of states of orientation throughout wide stretches of time and space. An organism can only
stabilize and characterize a visual world with respect to his own actions
for a short time by making his displacements and directing his attention
in an immediate sensory context. Relations beyond the scope of immediate experience must be sustained by memory.
Moreover, exploration of a set of relations in thought may be carried
out in some representation of the behavioral field which is not sustained
at all by visual effects, even within memory. I t is probable that, in
thought, description is primarily in terms of more intimate or selfsensing (proprioeeptive) reafference than vision provides.
Thus, the vision of space is not the only context for visual perception. Vision is, after all, only one highly articulate and fluent agent of
active behavior, functioning at its best in the sorting and relating of
Two Mechanisms of Vision in Primates
333
m a n y c o m p l e x d e t a i l s i n a field w h i c h e x t e n d s far a n d is full i n b r o a d
d a y l i g h t , is i m p o v e r i s h e d a t d u s k , a n d falls to n o t h i n g i n d a r k n e s s .
References
AJU~IAGUER~A, J., and It. H]~oAJ~: Le Cortex C6r~bral, 2nd edit. Paris: Masson &
Cie. 1960.
AKERT, K. : Experimenteller Beitrag betr. die zentrale Netzhaut-Representation
im Tectum Opticum. Schweiz. Arch. Neuro]. Psychiat. 64, 1--16 (1949a).
- - Der Visuelle Greifreflex. ttelv, physiol. Pharmaco]. Acta 7, 112--134 (1949b).
APT~, J. T. : Projection of the retina on the superior collieulus of eats. J. Neurophysiol. 8, 123--134 (1945).
- - Eye movements following strychninizationofthesuperioreolliculusof cats. J.Neurophysiol. 9, 73-86 (1946).
B~K~Sr, G. v. : Sensory Inhibition. Princeton: Princeton University Press 1967.
BE~DE~, M. B., and S. S~ANZ~R: Oculomotor pathways defined by electric stimulation and lesions in the brainstem of monkey. I n : M. B. BENDER (ed.), The
Oculomotor System, chap. 4, p. 81--140. New York: Harper & Row, Hoeber
Medical Division 1964.
BishoP, A. : Use of the hand in lower primates. In: J. BtrETTNER-JaN~rse~ (ed.),
Evolutionary and genetic biology of primates, vol. 2, p. 133--225. New York:
Academic Press 1964.
BLAKe, L. : The effect of lesions of the superior colliculus on brightness and pattern
discrimination in the cat. J. comp. physiol. Psyehol. 52, 272--278 (1959).
BoY~-ToN, R. M. : I n : Visual search techniques. Nat. Acad. Sei.-Nat. Res. Council
Publ. No. 712, 232 (1960).
BV~TTNER-JANVSe~, J.: An introduction to the primates. In: J. BgET~NERJANUSCg (ed.), Evolutionary and genetic biology of primates, vol. 1, p. 1--64.
New York: Academic Press 1964.
B u ~ R , C. M., and W. L. GE~:OZS~CI:Alterations in pattern equivalence following
inferotemporal and lateral striate lesions in rhesus monkeys. J. comp. physiol.
Psychol. 61, 309--342 (1966).
- - M. MIs~xr~, and H. E. ROSVOLD: Stimulus generalization following inferotemporal and lateral striate lesions in monkeys. In: D. 3/IosTOFSKY(ed.), Stimulus generalization. Stanford: Stanford University Press 1964.
CowE~, A.: Projection of the retina onto striate and prcstriate cortex in the
squirrel monkey, Saimiri sciureus. J.Neurophysiol. 27, 366--393 (1964).
- - , and L. W~SKR~SrrZ: A comparison of the effects of inferotemporal and striate
cortex lesion on the visual behavior of rhesus monkeys. Quart. J. exp. Psychol.
19, 246--253 (1967).
C~IG, W. : Appetites and aversions as constituents of instinct. Biol. Bull. 34, 91-107 (1918).
D ~ I n L , P. M., and D. W ~ T ~ I D G ~ : The representation of the visual field on the
cerebral cortex in monkeys. J. Physiol. (Lend.) 1~9, 203--221 (1961).
Dn~Y-BRow~, D. : The midbrain and motor integration. Prec. roy. Soc. Med.
55, 527--538 (1962).
- - , and t~. A. C~n~BEnS: Visuo-motor function in the cerebral cortex. J. ncrv.
ment. Dis. l~l, 288--289 (1955).
- - J. S. MEYm~, and S. H O I ~ S T ~ :
The significance of perceptual rivalry
resulting from parietal lesions. Brain 7~, 433--471 (1952).
D~VA~o~s, 1%. L. : Neural processing of visual information. In: R. W. RussEs~ (ed.),
Frontiers in physiological psychology, chap. 3, p. 51--91. New York: Academic
Press 1966.
334
C.B. TREVARTHEN:
Do~Y, R. W. : Functional significance of the topographical aspects of the retinocortical projection. In: R. Ju~G and H. KO~n~SBER (eds.), The visual system:
Neurophysiology and psychophysics, p. 228--245. Berlin-GJttingen-Heidelberg: Springer 1961.
Dow~E~, g. L. ])~ C. : Role of corpus eallosum in transfer of training in Macaca
muIatta. Fed. Prec. 17, 37 (1958).
- - Changes in visually guided behaviour following midsagittal division of optic
chiasm and corpus callosum in monkey (Macaca mulatta). Brain 82, 251--259
(1959).
~ISCn-MA~, M. W., and T. It. M]~IKL]~: Visual intensity discrimination in cats after
serial tectal and cortical lesions. J. comp. physiol. Psychol. ~9, 193--201 (1965).
G~z~, R. M., and M. JAconso~: The projection of the binocular visual field on the
optic tecta of the frog. Quart. J. exp. Physiol. 47, 273--280 (1962).
GAZZA~ICA, M. S., g. E. BOOE:% and R. W. SPER~r: Some functional effects of
sectioning the cerebral eommissures in man. Prec. nat. Acad. Sci. (Wash.) 48,
1765--1769 (1962).
- - - - - - Cerebral mechanisms involved in ipsilateral eye-hand use in split-brain
monkeys. Exp. Neurol. 1O, 148--155 (1964).
- - - - - - Observations on visual perception after disconnection of the cerebral
hemispheres in man. Brain 88, 221--236 (1965).
G~BSO~, J. J.: The senses considered as perceptual systems. Boston: Houghton
Mifflin 1966.
HAMPTOn, C. R., and M. S. GAZZANIGA:Lateralization of learning of colour and
brightness discriminations following brain bisection. Nature (Lend.) 201, 220
(1964).
H~a~RIS, A. J. : Eye movements of the dogfish Squalus acanthias L. J. exp. Biol. 48,
107--130 (1964).
HASSLER, ]:~.-" Comparative anatomy of the central visual systems in day- and
night-active primates. In: R. HASSLER and It. STEPm~ (eds.), Evolution of the
forebrain, p. 419--434. Stuttgart: Georg Thieme 1966.
H~CA~, H., and J. AJURIAGUnRRA: Balint's syndrome and its minor forms.
Brain 77, 373--400 (1954).
H~ss, R. W., S. BuRoI, and V. B v c ~ :
Motorische Funktion des Tektal- und
Tegmentalgebietes. Mschr. Psychiat. Neurol. 112, 1--52 (1946).
HUMPttR]~Y,N. K., and L. W]~ISKRANTZ:Vision in monkeys after removal of the
striate cortex. Nature (Lend.) 215, 595-597 (1967).
HYDe, J. E., and S. G. ELIASSON: Brainstem induced eye movements in cats.
J. comp. Neurol. 108, 139--172 (1957).
JACOBS]~, C. F. : Function of frontal association area in primates. Arch. Neurol.
Psychiat. (Chic.) 88, 558--569 (1935).
- - J. B. WOLF, and T. A. J~cKso~: An experimental analysis of the functions of
the frontal association areas in primates. J. herr. merit. Dis. 82, 1--14 (1935).
JAcoBsen, M.: The representation of the retina on the optic rectum of the frog.
Correlation between retino-tectal magnification factor and retinal ganglion cell
count. Quart. J. exp. Physiol. 47, 170--178 (1962).
I~iiVER, H. : Functional significance of the genieulo-striate system. Biol. Symposia
7, 253--299 (1942).
Kvu
H. G. J. M. : Discussion. In: V. B. MOV~TCASTLE(ed.), Interhemispheric
relations and cerebral dominance, p. 114---115. Baltimore: The Johns Hopkins
Press 1962.
- - M . K. SZW~CB)_~T, M. MISH~I~, and H. E. RosvoL~: Occipito4emporal
cortico-cortieal connections in the rhesus monkey. Exp. Neurol. 11, 245--261
(1965).
Two Mechanisms of Vision in Primates
335
LASHLEY,K. S. : The mechanism of vision: XVIII. Effects of destroying the visual
"associative areas" of the monkey. Genet. Psychol. Mono~. 37, 107--166
(1948).
LEE-TENG, E., and R. W. SPERRY: Intermanual stereognostic size discrimination
in split-brain monkeys. J. comp. physiol. Psychol. 62, 84--89 (1966).
LISSAUE~, W. : Ein Fall yon Seelenblindheit nebst eincn Bcitrag zur Theorie derselben. Arch. Psychiat. Nervenkr. 21, 222--270 (1890).
LORENZ, K. Z. : i3ber die Bildung des Instinktbegriffes. Naturwissenschaften 25,
289--300 (1937).
LucIA, A. R. : Disorders of "simultaneous perception" in a case of bilateral occipital
brain injury. Brain 82, 437--449 (1959).
- - Higher cortical functions in man. New York: Basic Books, Consultants Bureau
1966.
- - B. A. KA~I'OV, and A. L. YA~BUS : Disturbances of active visual perception with
lesions of the frontal lobes. Cortex 2, 202--212 (1966).
MACKWORT~, N. H.: Visual noise causes tunnel vision. Psychon. Sci. 3, 67--68
(1965).
~/[EIKLE, T. It. : Failure of interocular transfer of brightness discrimination. Nature
(Lond.) 1243--1244 (1964).
- - , and J. A. SECHZER: Interocular transfer of brightness discrimination in "split
brain" cats. Science 1~2, 734--735 (1960).
M~S~KIN, M. : Visual mechanisms beyond the striate cortex. In: R. W. RVSSELL
(ed.), Frontiers in physiological psychology, chap. 4, p. 93--119. NewYork: Academic Press 1966.
- - , and K. It. PRIBRAM: Visual discrimination performance following partial ablations of the temporal lobe: I. Ventral vs. lateral. J. comp. physiol. Psychol.
47, 14---20 (1954).
- - - - Analysis of the effects of frontal lesions in monkey. I. Variations of delayed
alternations. J. comp. physiol. Psychol. 48, 4 9 2 - 4 9 5 (1955).
- - - - Analysis of the effects of frontal lesions in monkey: II. Variations of delayed
response. J. comp. physiol. PsychoL 49, 36--40 (1956).
MYERS, R. E. : Function of corpus callosum in interocular transfer. Brain 79,
358--363 (1956).
-Corpus eallosum and visual gnosis. In: Brain )lechanisms and Learning. A
symposium, p. 481--505. Oxford: Blackwell Sci. Pub]. 1961.
- - Commissural connections between occipital lobes of the monkey. J. comp.
Neurol. 118, 1--16 (1962).
NAPIEr, J. R.: Studies of the hands of living primates. Proc. zool. Soc. London
184, 647--657 (1960).
- - Prehensility and opposability in the hands of primates. In: J. E. I-IARRIS (ed.),
Vertebrate locomotion, p. 115--132. Symposium No 5. London: Zool. Soc.
London 1961.
OSTE~m~Rr G. : Topography of the layers of rods and cones in the human retina.
Acta ophthal. (Kbh.) 65, Suppl., 1--102 (1935).
PASIK, P., and T. PASIK: Oculomotor functions in monkeys with lesions of the
cerebrum and the superior colliculi. In: M. B. BENDE~ (ed.), The oculomotor
system,chap. 3, p. 40--80. New York: Harper & Row, Hoeber Medical Division
19649.
PASIK, T., and P. PASIK: Optokinetic nystagmus: an unlearned response altered by
section of chiasma and corpus ca]losum in monkeys. Nature (Lond.) 203,
609---611 (1964b).
- - P. PAsn% and iYl. B. BEN])ER: The superior colliculi and eye movements. Arch.
Neuro]. (Chic.) l& 4 2 0 ~ 3 6 (1966).
336
C.B. TREVARTHEN:
PnlBEAM, K. H. : A review of theory in physiological psychology. Ann. Rev. Psychol.
11, 1--40 (1960).
- - , and M. M I s ~ I N : Analysis of the effects of frontal lesions in monkey: III. Object alternation. J. comp. physiol. Psychol. 49, 41--45 (1956).
t~ASEBASS, C. : The relationship between saccadie and smooth tracking eye movements. J. Physiol. (Lend.) 159, 326--338 (1961).
SANDERS, A. F.: The selective process in the functional visual field. From Inst.
for Perception I~V0-TNO, Nat. Def. t~es. Organization TNO. Soersterberg,
Netherlands, 1963.
SC~VASSMA~N, H. D., and L. KICUGER: Organization of the visual projection upon
the optic rectum of some fresh water fish. J. eomp. Neurol. 124, 113--126
(1965).
SI~INO~F, 1~., H. D. SCR-~VASSMA~,and L. KRUGEn : An electrophysiological study
of the visual projection to the superior colliculus of the rat. J. comp. Neurol. 127,
435--444 (1966).
S P E ~ u R. W. : Neurology and the mind-brain problem. Amer. Sci. 40, 291--312
(1952).
- - Corpus callosum and interhemispheric transfer in the monkey. Macaca mulatta
(abstract). Anat. Eec. 131, 297 (1958).
- - Cerebral organization and behavior. Science 133, 1749--1757 (1961).
SeRAGU]~, J. M.: Interaction of cortex and superior collicuins in mediation of
visually guided behavior in the cat. Science 153, 1544--1547 (1966).
- - , and T. H. MEI~LE jr. : The role of the superior colliculus in visually guided
behavior. Exp. Neurol. 11, 115--146 (1965).
TALBOT, S. A., and W. H. MARS11ALn:Physiological studies on neural mechanisms
of visual localization and discrimination. Amer. J. Opthal. 24, 1255--1264
(1941).
TEVBEn, H. L., W. S. BATTEI~SBY,and M. B. BE~DEn: Visual field defects after
penetrating missile wounds of the brain. Cambridge: Harvard Univ. Press 1960.
TI~EVARTHEN,C . B . : Studies on visual learning in split-brain monkeys. Unpublished
doctoral dissertation. California Institute of Technology. Pasadena 1962a.
-Double visual learning in split-brain monkeys. Science 136, 258--259 (1962b).
- - Proeessus visuels interh6misph6riques localis6s darts le trone c6r6bral. Leur mise
en 6vidence sur des singes ~ eerveau d6doubl6. C. ~. Soc. Biol. (Paris)157,
2019~2022 (1963).
- - Functional interactions between the cerebral hemispheres of the split-brain
monkey. In: E. G. ETTLINGEr~ (ed.), Functions of the Corpus callosum. Ciba
Foundation Study Group, No 20, p. 2 4 - 4 0 . And discussions, p. 103--106 and
p. 144--147. 1965.
- - Manipulative strategies of baboons and the origins of cerebral asymmetry. In:
M. KINSBOV~E (ed.), Hemispheric asymmetry of function. London: Tavistock
(1968)
VO~EIDA, T. J. : Performance of a visual conditioned response in split-brain cats.
Exp. Neurol. 8, 493--504 (1963).
WAG~A~, I. H. : Eye movements induced by electric stimulation of cerebrum in
monkeys and their relationship to bodily movements. In: M. B. BE~DE~ (ed.),
The oculomotor system, chap. 2, p. 18--39. New York: Harper & Row, Hoeber
Medical Division 1964.
W~LLS, G. L. : The vertebrate eye. Michigan: The Cranbrook Inst. of Science 1942.
- - The evolutionary history of eye movements. Vision Res. 2, 69--80 (1962).
W]~ISK~TZ, L. : Contour discrimination in a young monkey with striate cortex
ablation. Neuropsyehologia 1, 145--164 (1963).
Two Mechanisms of Vision in Primates
337
WELOlZ,K., and P. STUTV.VlLLE: Experimental production of unilatera] neglect in
monkeys. Brain 81, 341--377 (1958).
W]~I~TgEI~[, TJ~. : ~3ber die indirekte Sehsch~rfe. Z. Psychol. 7, 173--187 (1894).
WEYMOITT~, F. W. : Visual sensory units and the minimum angle of resolution.
Amer. J. Ophthal. 46, 102--113 (1958).
W~IITT~RIDGE, D. : Area 18 and the vertical meridian of the visual field. In: E. G.
ETTLI~GSR (ed.), Functions of the Corpus eallosum. Ciba Foundation Study
Group, No 20, p. 115--120. London: Churchill 1965.
WILsOn, W. A., and M. MIS~KII~. Comparison of the effects of inferotemporal and
lateral occipital lesions on visually guided behavior in monkeys. J. comp.
physiol. Psychol. 5~., 10--17 (1959).
YAI~Bus, A. L. : Eye movements and vision. New York: Plenum Press 1967.
Dr. CoLwu162B. TI~EVAI~TIZE~
Harvard University
Cambridge, ~ass. USA