@ European Neuroscience Association 0953-81W 9 0 $3.00
European Journal of Neuroscience, Vol. 2 , pp. 369-377
Horizontal Interactions in Cat Striate Cortex: 111. Ectopic
Receptive Fields and Transient Exuberance of
Tangential Interactions
H. J. Luhmann’, J. M. Greue12 and W. Singer3
’
Universitat Koln, Physiologisches Institut, Albertus-Magnus-Platz, D-5000 Koln
41, FRG
*Troponwerke GrnbH, Berliner Str. 156, Postfach 80 10 60, 5000 Koln 80, FRG
3Max-Planck-lnstitutfur Hirnforschung, Deutschordenstr. 46, D-6000 Frankfurt
a.M. 71, FRG
Key words: visual cortex, receptive fields, development, deprivation
Abstract
In this study the developmental changes of intracortical connectivity are related to changes of cortical
receptor fields (RFs). The RFs of striate cortex neurons of 4- to 8.5-week-old kittens, reared under normal
conditions (NR) or in a selective visual environment (SE), were analysed quantitatively and compared with
adult cats. To unmask weak inputs from outside the conventional RF (CRF), cell excitability was raised by
iontophoretic application of glutamate (GLU) andlor bicuculline methiodide (BIC) or by light stimulation of the
CRF. Both the dominant discharge region (DDR) and the total RF (TRF) area were significantly larger in NR
and SE kittens than in adult cats. Moreover, in kittens 18% of the cells had additional ectopic fields that
were excitatory, had similar orientation preferences as the CRF, and ranged 4 O to 23O from the centre of the
CRF. In 74% of the cases the ectopic fields were direction-selective and 70% of them preferred stimuli
moving toward the CRF. Ectopic fields occurred mainly in supragranular cells, were similarly frequent in
simple and complex cells and slightly more frequent in SE (20.7%) than in NR (13.3%) kittens. In adult cats
only one of 83 cells tested had an ectopic field. It is concluded that the age-dependent decrease in the RF
size, the laminar distribution of cells having an ectopic RF, and the numerical reduction of these cells with
age correlate well with the organization and postnatal pruning of tangential projections, suggesting that these
contribute to the elaboration of specific response properties. Moreover, the authors infer from the early
presence and from the selectivity of ectopic fields that the system of horizontal intrinsic connections mediates
far-reaching, excitatory interactions between cortical neurons with similar functional properties and serves as
a substrate for the processing of global aspects of visual patterns.
Introduction
The existence of far-reaching tangential connections in striate cortex
suggests that the area in the visual field from which neuronal responses
can be influenced exceeds that predicted by the spatial overlap of
thalamo-cortical terminal arbors (for review see Ferster and Lindstrom,
1984; Nelson and Frost, 1985). Therefore, influences mediated by
intrinsic tangential connections ought to come from regions outside
the conventional receptive field (CRF). Such long range effects have
been searched for in numerous studies, but most authors agree that
they are weak and infrequent. The peripheral stimuli either had to be
very large and moving or they had to be presented in conjunction with
stimuli placed within the CRF in order to show an inhibitor or
facilitatory influence on the cellular activity (Fries and Albus, 1973;
Gulyas et al., 1987; Hammond and MacKay, 1981; Jones, 1970; Maffei
and Fiorentini, 1976; Nelson and Frost, 1985; Orban et al.. 1987;
Rizzolatti and Camarda, 1977). It has been further suggested that some
of the very large CRFs can only be accounted for if one assumes a
contribution of far-reaching tangential connections. This has been
proposed to be the case for the very elongated fields of layer VI cells
(Gilbert, 1977; Gilbert and Wiesel, 1983) and particularly for wide
RFs consisting of several excitatory subregions (Nelson and Frost,
1985; Pollen and Ronner, 1975). In the preceding two papers (Luhmann
et al., 1990a, b), the author presented data which indicate that tangential
connections are more numerous and mediate excitatory synaptic actions
more effectively over larger distances in kittens than in adult cats. This
suggests that remote influences on cortical responses might be more
readily detectable in striate cortex of kittens. This conjecture receives
direct support from an earlier study that was performed in kittens raised
with selective visual experience (Singer and Tretter, 1976). In this study
Correspondence to: W . Singer, as above
Received 11 April 1989, revised 5 December 1989, accepted 11 December 1989
370 Ectopic receptive fields in cat area 17
neurons were encountered which possessed, in addition to the CRF,
further ectopic regions clearly separated by 10" to 20°C from the centre
of the CRF. These ectopic fields produced strong responses even when
stimulated alone and based on theoretical arguments it was concluded
that they resulted from experience-dependent selective stabilization of
intracortical connections (Singer, 1985a, b).
In the present study we investigated the possibility that these farreaching tangential interactions are also more readily demonstrable in
NR kittens than in adult cats. For that purpose we quantitatively
analysed the receptive fields (RFs) of a large number of cells in striate
cortex of NR kittens, of kittens reared with selective visual experience,
and of NR adult cats.
Part of this work has been presented in abstract form (Luhmann et
al., 1987).
TABLE1. Summary of investigated cats
Animal
Animals and procedure
This study is based on 20 cats. Their respective ages and rearing
conditions are summarized in Table 1.
Eight kittens (NR-A-NR-H) and five adult cats (NR-J -NR-M) were
bred in our cat colony and reared under normal conditions. Seven more
kittens (SE-A-SE-G) were transferred into a dark room before natural
eye opening and from the middle of the fifth postnatal week onwards
were exposed selectively to vertical gratings of constant spatial
frequency. For that purpose kittens were transferred every day for
1-4 h to a 2 m wide and 1.1 m high cylinder, which was covered
inside with a high-contrast pattern of vertically oriented black and white
stripes. During exposure kittens wore masks constructed of
polyurethane foam which were fixed to the arms of a carousel similar
to that described by Held and Hein (1963). This procedure prevented
the kittens from seeing their paws and the horizontal border of the
vertical pattern and assured constant viewing distance of 36 cm from
the cylinder. At this distance, the black bars covered a visual angle
of 3 O and the distance between them was 5 " . Total exposure time ranged
from 31 to 67 h (Table 1). To minimize the influence of any other
visual stimulation, animals were transported from the dark room to
the exposure apparatus in a small light-impermeable box and masks
were fixed on the kittens' heads in complete darkness. All animals
reared in a selective visual environment (SE-A -SE-G), were
anaesthetized in the dark room and then prepared for
electrophysiological recordings.
Preparation and electrophysiology
For surgical preparation, animals received i.m. injections of 0.01 mg
atropine sulphate and a mixture of 30 mg/kg ketamine hydrochloride
and 15 mglkg xylazine hydrochloride. During further preparation and
recording, anaesthesia was maintained by artificial ventilation with a
mixture of N20/02 (70:30) and by a continuous i.v. infusion of 6%
pentobarbital (1.8 mg/kg X h) or by adding 0.2-0.4% halothane. At
the end of all surgical procedures, the animals were paralyzed with
an i.v. infusion of 0.7 mg/kg X h hexacarbacholine bromide. A 5%
glucose-Ringer's solution (5: 1) was given continuously at a rate of
3 -6 ml/h through an orally inserted gastric catheter. During recording,
EEG, heart rate, body temperature and the expiratory C02 were
monitored continuously. Rectal temperature was held constant at
37.5"C and tidal volume and rate of respiration were adjusted to yield
end-tidal C02 concentrations between 3.5 and 4%. The pupils were
dilated with atropine, the nictating membranes retracted with
Age
[weeks]
Number of
qualitatively
analysed
cells
NR-A
NR-B
NR-C
NR-D
NR-E
4
4.5
NR-F
5
5.5
25
7
adult
adult
adult
adult
adult
6
6.5
7
7
7
8
8.5
24
21
NR-G
NR-H
NR-I
NR-J
NR-K
Materials and methods
Visual
experience
[hours]
NR-L
NR-M
SE-A
SE-B
SE-C
SE-D
SE-E
SE-F
SE-G
31
24
5
33
16
5
5
5
33
17
-
31
40
10
46
50
60
67
16
15
14
56
60
Number of
quantitatively
analysed
cells
9
17
3
18
6
5 , 7+
13
5
5
13
1
12
8
7
16
49
49
14
1
65
35
15
12
20
II
The age of normally reared (NR)animals and kittens raised in a .selective visual environment
(SE) at the time of recording is given in weeks. Cats older than 6 months were classified
as adult. For animals reared in a restricted visual environment. the total exposure time
is indicated in hours. The last two columns give the number of qualitatively and
quantitatively analysed cells for each animal. Units. which were investigated with stationary
stimuli. are indicated by (see kitten NR-F).
+
neosynephrine and the corneas protected with contact lenses containing
artificial pupils of 2 mm diameter. The refractive state of both eyes
was determined by a refractometer and refractive errors were corrected
by appropriate spectacle lenses. With a fundus camera, the retinal
landmarks were plotted on a tangent screen located 1.14 m in front
of the cat's eye plane. Single cell activity was recorded with a
micropipette containing 1.5 M potassium citrate. For iontophoretical
application of drugs, a seven-barrelled micropipette was glued to the
recording electrode. The cortex was covered with silicone or 4%agar
and the skull opening sealed with bone wax to avoid drying out and
to minimize pulsations. Multibarrelled electrodes were filled with 0.1 M
glutamate (GLU), pH 8.5,5 mM bicuculline methiodide (BIC), pH 3.0,
and 2.0 M NaCl which served as balance. DC resistance of the
recording electrodes ranged from 10 to 30 M62 and electrode signals
were fed into a conventional FET-equipped input stage of an amplifier
system.
Visual stimulation and iontophoresis
Receptive fields were qualitatively analysed with hand projected light
stimuli of variable width and length. The background luminance was
0.2 cd/m2 and the stimulus luminance 22 cd/m2. For detailed
quantitative investigation, the authors used electronically controlled
light stimulators and peristimulus-time histograms (PSTHs) were
computed on-line from responses to repeated stimulus presentations.
Neurons with little or no spontaneous activity were often detected by
moving a stimulus with properties preferred by the last recorded cell
continuously over the tangent screen. In order to reveal subliminal
facilitatory and inhibitory inputs to the recorded cells and to detect
remote influences from outside the CRF, the authors used the dual
stimulus technique (Bishop er al., 1971a; Orban er al., 1979) or
Ectopic receptive fields in cat area 17 371
iontophoretically applied GLU (Hess and Murata, 1974) andlor BIC
(Sillito, 1975) through one or several of the iontophoresis barrels. The
retaining current for GLU was 10 nA and for BIC - 10 nA. Ejection
currents ranged from -5 to -20 nA for GLU and from + 5 to +50
nA for BIC.
+
Cell classification and quantitative analysis
Whenever a neuron was isolated, the following parameters were
routinely determined: (i) recording depth from cortical surface; (ii) the
cell's spontaneous activity; (iii) the orientation, the movement velocity
and direction, and the length of the stimulus that gave maximal
responses; (iv) the vigour of the left and right eye response to an optimal
stimulus, using the criteria of Greuel et al. (1987) for classification;
(v) the ocular dominance (OD) according to a scale of 5 classes (1
and 5: monocular; 2 and 4: binocular with unilateral bias; 3: binocular
without bias); (vi) the spatial structure of the RF (simplelcomplex) as
determined from responses to stationary stimuli of optimal orientation;
(vii) the orientation tuning in steps of 22.5"; and (viii) the size of the
RF. Once this analysis was completed, visual stimuli of different lengths
and orientation were moved over a wide area of the visual field in search
for any remote influences on the cell's discharge behaviour. Moving
stimuli were used because they provide a more accurate estimate of
the spatial organization of the RF (Kulikowski and Bishop, 1981) and
are more successful in revealing remote responses from outside the
CRF than stationary stimuli (Andrews and Pollen, 1979). However,
in seven neurons (Table I, kitten NR-F) the authors also analysed in
detail the RFs with stationary stimuli positioned at different locations
in the visual field. To reveal weak influences, responses were averaged
from up to 50 stimulus passages. The following RF dimensions were
defined for quantitative comparison: (i) width of the excitatory dominant
discharge region (DDR) which gave the strongest response in the PSTH;
(ii) width of the total receptive field (TRF) including all excitatory and
inhibitory subregions; and (iii) existence of an ectopic field. The criteria
were that the additional field was clearly segregated from the CRF
and separated by more than 4" from the CRF (Singer and Tretter,
1976).
Statistical analysis
A Lilliefors-test (Lilliefors, 1967) on normality and a linear or nonlinear
regression analysis were performed to analyse the relation between
RF size and RF eccentricity. The significance of the correlation
coefficient was tested with a t-test. Groups were compared with a
X2-test or a nonparametric Wilcoxon-Mann-Whitney U-test with
different significance levels.
Results
Comparison of RF size in kittens and adult cats
The authors analysed a total of 608 neurons in the primary visual cortex
of eight NR kittens, five NR adult cats and seven SE kittens (Table 2).
A detailed quantitative analysis of the RF dimensions was carried
out on 204 units. In 144 cells (71%), the RF structure was examined
only with moving light bars. Stationary stimuli were used in another
seven of the investigated neurons (3%). In order to increase the
probability of detecting weak influences from outside the CRF the
authors applied iontophoretically BIC to 18 of the cells (9%) and a
combination of GLU and BIC to 27 units (13%). In eight neurons (4%),
the cell's activity was increased by continuously moving a conditioning
TABLE2. Summary of RF dimensions in kittens and adult cats
DDR width
TRF width
["I
["I
Kittens
simple; NR; no BIC/GLU
simple; NR; with BIC/GLU
simple; SE; no BIC/GLU
complex; NR; no BIC/GLU
complex; NR; with BIC/GLU
complex; SE; no BIC/GLU
2.8* 1.4 (9)
3.3 h 1.6 (27)
1.5*0.9 (34)
5.7*.1.8 (20)
5.4*3.5 (18)
3.0=k2.1 (47)
5.9*4.5
5.6+2.8
2.7 f I .9
6.2h1.8
7.2*3.6
4.7+2.8
Adult cats
simple; NR; no BIClGLU
complex; NR; no BIClGLU
1.3 *0.9 (23)
3.6*1.6 (16)
2.6* 1.7 (23)
3.6*1.6 (16)
Cell group
~~~
(10)
(28)
(34)
(21)
(18)
(48)
For each experimental group (see materials and methods), the mean width +SD of the
dominant discharge region (DDR) and the total receptive field (TRF) is given. The numbers
in parentheses indicate the number of cells analysed in each group. For abbreviations see
text.
stimulus within the CRF. The CRFs of all units were located within
20" of the area centralis.
In NR kittens the mean width of the DDR was significantly smaller
(U-test, p < 0.001) in simple (2.8 f 1.4" SD, n = 9) than in complex
cells ( 5 . 7 f 1 . 8 " SD, n = 20). No significant difference was found
between the two cell groups with respect to the mean width of the TRF
(p < 0.01 level; TRF width of simple cells: 5.9 k4.5" SD, n = 10;
TRF width of complex cells: 6.2 f 1.8" SD, n = 21). In SE kittens,
the DDR width was also significantly smaller (p < 0.001) in simple
cells (1.5f0.9" SD, n = 34) than in complex cells (3.0k2.1" SD,
n = 47); however in contrast to NR kittens, the mean width of the
TRF was also significantly smaller (p < 0.001) in simple (2.7 f 1.9"
SD, n = 34) than in complex cells ( 4 . 7 ~ t 2 . 8 "SD, n = 47). In SE
kittens, all parameters referring to RF size of both simple and complex
cells gave significantly smaller values than in NR kittens. For simple
cells the DDR and TRF values were different at the p < 0.01 level;
for complex cells DDR values differed at the p < 0.001 level and TRF
values at the p < 0.01 level. Iontophoretic application of BIC and GLU
caused only a small increase in the mean width of the DDR and TRF,
which neither in simple nor in complex cells reached the level of
statistical significance (for all parameters: p > 0.1).
In NR adult cats, DDR and TRF widths were smaller than in NR
kittens both for simple and complex cells. The DDR and the TRF of
simple cells measured 1 . 3 ~ t 0 . 9 "SD (n=23) and 2 . 6 k I . 7 " SD
(n=23), respectively and differed from the corresponding values in
NR kittens at the p<O.OI level. For complex cells of adult cats, the
width of the DDR and TRF are taken as identical, because the authors
were not able to demonstrate multiple excitatory subregions, or
inhibitory sidebands, as they have been described for a small number
of complex cells by other authors (Albus and Fries, 1980). The fields
of complex cells in adult cats measured 3 . 6 ~ k 1 . 6 "SD (n=16) and
differed from those in NR kittens at the p <0.01 (DDR) and p <0.001
(TRF) level.
Responses from outside the conventional receptive field
Responses separated by more than 4" from the centre of the CRF were
detectable only with moving stimuli. In seven neurons, the region
around the CRF was thoroughly explored with stationary stimuli, but
none of these cells showed a response to ectopic stimuli.
In kitten striate cortex, 18% (n=28) of the units had one or two
372 Ectopic receptive fields in cat area 17
t
1
A
I lB
FIG.1. Example of a simple cell in area 17 of a 5-week-old NR kitten (NR-D)
with a direction- and orientation-specificectopic field (open arrow in PSTH
A). The cell was recorded in a depth of 237 pm below the pial surface, was
binocular and rated in OD class 4. Its CRF (DDR width: 3.1 O ; TRF width:
6.9") had an eccentricity of 4", showed a preference for a horizontally oriented
stimulus and was direction-selective, responding stronger to a downward than
to an upward moving bar (see PSTH A). Stimulation with an optimally-oriented
bar revealed an additional ectopic field (width: 4.79, which was located 14.8"
below the centre of the CRF. The ectopic field showed the same orientation
preference as the CRF and was highly direction-selective. Whereas the CRF
responded stronger to a downward moving bar, the ectopic field responded only
to an upwards moving stimulus (PSTH A). Iontophoretic application of BIC
( f 5 nA) during the quantitative investigation of this cell caused a loss in the
orientation specificity of the CRF. The orientation of the stimulus and its direction
of movement are indicated below the PSTHs by bars and arrows, respectively.
Plots of the RF sbllcture (diagramson the right) were obtained from the responses
to an optimally-orientedstimulus (PSTH A) and an orthogonal-oriented stimulus
(PSTH B). Stimulus-evokedexcitatory responses are indicated by dotted regions,
inhibitory subregions within the CRF are shown as clear regions. The upper
diagram illustrates the responses elicited from the CRF (1) and the ectopic field
(2) by an upwards moving horizontal stimulus and a vertical stimulus moving
from left to right. The lower diagram shows the response to stimuli moving
in the opposite direction. The position of the area centralis is indicated by a
dot. Stimulus velocity was 6.7"/s and vertical calibration indicates 5 spikes175 ms
bin. PSTHs A and B are based on 20 epochs with a cycle length of 20 s. In
each epoch the stimulus was moved for 6 s in one direction and then after a
delay of 2 s was moved backwards for 6 s along the same trajectory. The average
level of spontaneous activity was estimated from the discharge rate in the last
6 s of each PSTH.
ectopic fields. The percentage of neurons with an ectopic response was
higher in SE kittens (20.7%,n = 17) than in NR kittens (13.3%, n = 1l),
but this difference was not significant (p>O.O5, X2-test). Of the cells
with an ectopic field, ten (36%) had a C R F of the simple and 18 (64%)
of the complex type. One simple and two complex cells had two ectopic
fields. In 45 quantitatively analysed neurons in SE and NR kittens,
the authors raised the discharge level with iontophoretic application
of GLU and BIC or with continuous stimulation of the C R F in order
to detect remote inhibitory influences. However, in no case could they
demonstrate any far-reaching suppressive effects from regions outside
the CRF. All ectopic fields were excitatory.
A n example of a simple cell with a one direction-selective ectopic
field is shown in Figure I . The ectopic field (open arrow in Fig. 1A)
had a diameter of 4.7" and was located 14.8" below the CRF. The
FIG.2. Receptive field properties of a binocular (OD class: 2) cell with two
ectopic fields. The cell was recorded in the medial bank of area 17 in a depth
of 4971 pm from a 5-week-old kitten (NR-C). The CRF of the cell had complex
properties, was oriented horizontally and broadly tuned (*90").It was located
at an eccentricity of 17" and was about 15.5" wide and 12" long. In addition,
there were two highly direction-selective ectopic fields, which were located
16" to the left (field I) and 13" to the right (field 3) of the CRF (field 2). All
responses in this figure were obtained while BIC ( + 5 nA) was continuously
applied to the cell. PSTH A shows the response to a 30" long and 0.5" wide
horizontal bar moving up and down, PSTHs B-D represent the cell's response
to vertical bars of different length (34" in B, 5" in C and D) moving horizontally.
The direction of movement is indicated below each histogram by small arrows.
The photograph from the oscilloscope screen shown in the lower left has been
taken during the recording of PSTH C and indicates the trapezoidal signal, which
corresponds to stimulus motion and position, and the DC-signal, which shows
the cell's responses to stimulation of fields 1, 2 and 3. Each PSTH is based
on 50 epochs with a cycle length of 20 s. Stimulus velocity was 6.5"/s, vertical
calibration indicates 100 spikes/l50 ms bin. Note the different scales for angular
distance in the plots of the RF and the PSTHs.
optimal stimulus of the C R F was a horizontal oriented bar, but during
the application of iontophoretically applied BIC, responses to an
orthogonal, vertical stimulus could also be obtained (Figure 1B). The
ectopic field was strongly orientation- and direction-selective and
responded only to a horizontal stimulus moving toward the C R F
(Fig. 1A).
As illustrated in Figure 2, a cell could also have two ectopic fields.
This cell had a complex CRF, responded strongest to an upward moving
horizontal bar (PSTH A in Fig. 2), and was broadly tuned. The CRF
was 15.5" wide, 12" long and located at an eccentricity of 17". The
spatial organization of the R F was investigated quantitatively during
iontophoretic application of BIC ( + 5 nA) and by stimulation with
optimal and nonoptimal oriented bars of different lengths. In addition
to the CRF, the neuron had two ectopic fields, which were located
16" left (field 1 in R F plot of Fig. 2) and 13" right (field 3) from the
centre of the CRF (field 2). Ectopic field 1 had a diameter of 4.5"
Ectopic receptive fields in cat area 17 373
25
-
20
-
10
-
A
O
n
1
5
15
-
10
-
15
T
--
5-
0-i
FIG. 3.
(A) distance between ectopic and CRFs plotted as a function of CRF
eccentricity. The horizontal broken line indicates the distance from the CRF
(4")beyond which additional excitatory RF regions were considered as ectopic.
Simple cells are symbolized by circles, complex cells by quadrangles. Units
which were analysed during application of BIC, GLU are represented by filled
symbols. Symbols connected by vertical lines represent two ectopic fields
belonging to the same cell.
(B) mean distance between ectopic and classical R F s r SD in simple (circles)
and complex cells (quadrangles) investigated without (open columns) and with
iontophoretic application of BIC and/or GLU (filled columns). The number
above each column indicates the number of ectopic fields.
and its centre was situated 5" from the area centralis. Ectopic field
3 was 2" wide and located at an eccentricity of 30". Both ectopic fields
were highly direction-selective and both responded only to a vertical
stimulus, which moved in the direction toward the CRF. The size of
theectopicfieldsrangedfrom0.3 to5.8" (mean: 2.2*1.4" SD, n=31)
and did not differ for cells with simple or complex CRFs. Of the 31
ectopic fields, 84% (n=26) were orientation selective and 88% (n=23)
of these had the same orientation preference as the CRF. In the
remaining three cells, the orientation preferences between the ectopic
and the conventional field differed between 45" and 90".Seventy-four
percent (n=23) of the ectopic fields had a pronounced direction
selectivity and 70% (n= 16) of these preferred stimulus movements
towards the CRF. The CRFs of the 28 cells with an ectopic field showed
direction selectivity in 71 % (n=20), and in 45% of these units, the
CRF preferred the same stimulus direction as the ectopic field. Ocular
dominance was determined for ten ectopic fields and in seven of these
was found to be similar to that of the CRF.
The distances between ectopic fields and the CRF are plotted in
Figure 3A as a function of the retinal eccentricity of the CRF. Statistical
analysis revealed no significant linear relation between the two
parameters (t-test for correlation, p >O. I). There was, however, an
indication that particularly distant ectopic fields were more frequent
in cells with complex rather than simple CRFs. The mean distance
of ectopic responses was significantly larger (U-Wilcoxon-test,
p<0.05) in cells with complex CRFs (12.2 f 1.1" SD) than in cells
with simple CRFs (7.9 f 3 . 1 a SD). Moreover, the data indicate that
iontophoretic application of BIC andlor GLU increased the probability
to detect remote influences (Fig. 3B). Ectopic fields of cells, treated
with BIC and/or GLU were on the average located more distant from
the centre of the CRF (cells with simple CRF: 11.3+3.2" SD; cells
with complex CRF: 15.5 f 1.8" SD) than in untreated neurons (cells
with simple CRF: 6.7 f 2 . 0 " SD; cells with complex CRF: 11.1 f5.0"
-I
I-
-t
I
20°
1
1
0 sp.
4 sec
FIG.4. Receptive field structure of a binocular (OD class: 3) complex cell in
striate cortex of an adult cat (NR-J). The CRF (width: 5.5", length: 8") was
oriented horizontally with a tuning of *45", responded only to a downward
moving stimulus and was located at an eccentricity of 8.5". A direction-selective
ectopic field (width: 2". length: <5") was located 14" lateral from the CRF.
The response from the ectopic field was stronger for a stimulus moving upwards
in the direction of the CRF, than for a downward moving stimulus (see open
arrows in PSTH B). The ectopic field showed the same orientation preference
as the CRF. Stimulation with an orthogonal, vertically oriented stimulus revealed
no response from the ectopic field and only an inhibitory response from the
CRF (filled arrows in PSTH G). All PSTHs are based on 50 epochs, stimulus
velocity of 8"/s, and vertical calibration indicating ten spiked125 ms bin.
SD). However, this difference only reached the level of significance
in cells with simple CRF (U-Wilcoxon-test, p<0.05).
Cells with ectopic receptive fields were encountered preferentially
within the first 800 pm of each penetration, suggesting that they are
located mainly in supragranular layers. Of all the units analysed between
200 and 800 pm, which corresponds approximately to layers I1 and
111, 1 1% had an ectopic field, while this was the case for only 5 %
of the cells recorded between 800 and 1400 pm. The responses obtained
from the ectopic fields were more variable than those elicited from
the CRF. Occasionally even strong responses from ectopic fields would
suddenly disappear for a few minutes and reappear as unpredictably
as they vanished. These temporal variations were unrelated to any
external parameters that the authors could control such as the level
of halothane anaesthesia.
In primary visual cortex of adult cats, only one of 83 investigated
neurons had an ectopic field (Fig. 4). This ectopic field was located
14" from the centre of the CRF and had a diameter of 2". The CRF
and the ectopic field both preferred a horizontal stimulus (PSTH B-E
374 Ectopic receptive fields in cat area 17
in Fig. 4). Stimuli that were orthogonal to the preferred orientation
evoked no response from the ectopic field and only an inhibitory
response from the CRF (see arrows in PSTH G of Fig. 4). This
suppressive influence on the cell's resting discharge level by a
nonoptimal oriented stimulus passing over the CRF has been reported
previously (Sillito, 1979) and might be mediated by local inhibitory
lateral interactions between neighbouring cells having different
orientation preferences ('cross-orientation inhibition'; for review see
Sillito, 1984). The ectopic field and the CRF differed in their direction
selectivity. Whereas a response from the CRF could be evoked only
with a downward moving stimulus (PSTH C-E), the ectopic field
showed a preference for an upwards moving bar. Thus, as in kittens,
this ectopic field also responded preferentially to a stimulus moving
toward the CRF (PSTH B).
Discussion
Postnatal changes in receptive field dimensions
The mean values of the RF dimensions found in the present study are
in agreement with those described in earlier reports both for kitten
(Albus and Wolf, 1984; Braastad and Heggelund, 1985; Imbert and
Buisseret, 1975) and adult cat visual cortex (Albus, 1975; Heggelund,
1981a, b; Palmer and Davis, 1981; Rose, 1977). Also in agreement
with earlier reports (Braastad and Heggelund, 1985; Hubel and Wiesel,
1962; Palmer and Davis, 198I), the mean width of the DDR was found
to be larger in complex than in simple cells. However, this was not
true for the TRF. The authors propose that this is because simple fields
often possess distinct inhibitory sidebands, which contribute to the TRF
but not to the DDR (Bishop et al., 1971b, 1973), while complex cells
often lack an inhibitory sideband or subregion. Then DDR and TRF
often coincide (but see also Albus and Fries, 1980). Comparisons of
RF sizes in kittens and adult cats revealed that the DDR and TRF of
simple and complex cells were significantly larger in the former than
in the latter. The DDR and TRF width of simple cells was about twice
as large in NR kittens as in adults and the respective factor for complex
cells was 1.6 (see Table 2). This age-dependent decrease in RF size
may have several causes. It could result from pruning of thalamocortical axonal arbors that occurs during the early postnatal development
(LeVay et al., 1978). It could also be a consequence of the reduction
of intracortical long-range connections for which the authors obtained
indications in previous studies (Luhmann et al., 1986, 1990a). Finally,
increased inhibitory interactions could also contribute to a reduction
of RF size. At the present stage the authors cannot decide between
these possibilities, but several arguments suggest that the reorganization
of tangential intracortical connections may be causally related to the
reduction of RF size. The size of cortical RFs often exceeds
considerably the scatter of the geniculocortical projection, which led
Ferster and Lindstrom (1984) to suggest an involvement of horizontal
intrinsic connections in the formation of large RFs. If increased
inhibition were the sole cause of changes in RF size, one would expect
that the decrease occurred mainly for the DDR and not for the TRF,
because the latter comprises both excitatory and inhibitory subregions.
Because this was not the case, changes in cortical inhibition are probably
not alone responsible for the size changes. Furthermore, our analyses
of the RF dimensions in kitten striate cortex showed that both the mean
widths of the DDR and the TRF were significantly smaller in kittens
with restricted visual experience than in NR kittens (Table 2). This
difference may result partially from the fact that the SE kittens were
on average about 2 weeks older at the time of recording than the NR
kittens. However, it appears unlikely that the large differences of
1.3-3.2" in the mean widths of the DDR and TRF between NR and
SE kittens were solely age-dependent (Albus and Wolf, 1984; Braastad
and Heggelund, 1985). Plots of RF size versus eccentricity indicate
that the differences in mean RF width between these groups were
especially pronounced in the more peripheral representationof the visual
field at eccentricitics beyond 5 " , and less distinct at an eccentricity
between 0" and 5". Thus, restricting visual experience seems to affect
the central and peripheral representationsto a different extent. A similar
conclusion has been reached by Flood and Coleman (1979) on the basis
of anatomical studies.
Far-reaching lateral interactions
The systematic analysis of regions in the visual field remote from the
CRF revealed that in both NR and SE kittens a fraction of cells possess
ectopic RFs which were clearly separated from the CRF. Responses
from far outside the CRF were more readily obtained during
iontophoretic application of BIC and GLU (Fig. 3). Earlier reports
by Hess and Murata (1974) and Sillito (1975) already showed that such
treatment helps to reveal subliminal inhibitory or excitatory inputs to
cortical cells in vivo,and Miles and Wong (1987) demonstrated in the
in vitro guinea pig hippocampal slice preparation, that suppression of
inhibition with picrotoxin reveals excitatory connections between two
cells appearing as unconnected prior to treatment. The intracortical
long-range connections predominantly contact the distal parts of the
apical dendrite of pyramidal cells (see Luhmann et al., 1990b) and
BIC could uncover these remote inputs. However, i n 21 out of 28 cells
with an ectopic field, remote influences could also be detected without
application of GLU or BIC. Ectopic RFs have been found previously
in striate cortical neurons of kittens that had selective visual experience
with vertically oriented gratings (Singer and Tretter, 1976). The present
results extend these findings to NR kittens. The percentage of cells
possessing ectopic RFs and their laminar distribution is similar to that
described in the earlier study. Although the authors did not observe
a significant difference in the number of cells with an ectopic field
between SE and NR kittens, there was a tendency for a higher
percentage of ectopic fields in the former (20.7%) as compared to the
latter (13.3%). This trend is to be expected if, as proposed previously,
tangential intracortical connections are stabilized selectively by
patterned visual stimuli (Singer, 1985a, b). The conjecture is that
exposure to a simple, periodic visual pattern would lead to selective
stabilization of wide-spread lateral connections between cells that are
often activated simultaneously by the stripes of the grating.
The substrate of long-range interactions
To test the plausibility of the assumption that these ectopic responses
are mediated by intrinsic horizontal connections the authors estimated
the distance that these connections must span, by transferring the
positions of the CRF and of the ectopic fields on to a topographic map
of area 17 (Fig. 5A).
These measurements suggest that about 65% (n=20) of the 3 1 ectopic
fields required tangential projections spanning from 2 to 6 mm, the
extreme cases necessitating interactions over as much as 10 mm
(Fig. 5B). Such large distances cannot be spanned by the arborization
of thalamic afferents (Ferster and LeVay , 1978). The long-range
interactions, thus, must be attributed either to intra-areal tangential
connections or to feedback projections originating in other cortical
areas. The authors discuss the first possibility first. The RF properties
Ectopic receptive fields in cat area 17 375
FIG.5 .
(A) map of unfolded cat striate cortex, slightly modified from Tusa et al.
(1978) and kindly provided by Lowel et al. (1987). The representation of the
area centralis (filled dot), and of the vertical (VM) and horizontal meridian
(HM) is shown together with the positions of the CRFs and the ectopic fields
of the cells shown in Figure 2 (asterisks) and Figure 5 (dotted circles). The
corresponding distance of lateral interactions can be estimated from the calibration
bar.
(B) spatial extent of horizontal interactions in kittens (filled columns) and
in adult cats (dotted area) as revealed by the method shown in A.
of the ectopic fields are fully compatible with the assumption that the
remote input is provided by other striate cortex cells. The spatial spread
of tangential connections in kitten area 17 is also sufficient to mediate
interactions over distances such as are suggested by the present results.
As shown previously, they can span distances of up to 10.5 mm
(Luhmann et a l . , 1990a). Evidence is further available from electron
microscopic studies (Gabbott et al., 1987; Kisvarday et al., 1986) and
from the authors previous CSD analysis (Luhmann et al., 1990b) that
the far-reaching intracortical connections are excitatory. Finally, there
are good correlations between the laminar distribution of tangential
fibres and the location of cells with ectopic fields, and between the
age-dependent pruning of tangential connections and the reduction of
cells with ectopic fields in adult animals. The far-reaching tangential
connections were most prominent in supragranular layers and their
number (Luhmann er al . , 1986, 1990a) as well as the spatial extent
of excitatory effects mediated by these connections (Luhmann et al.,
1990b) becomes reduced with age. Available evidence is thus, without
exception, compatible with the hypothesis that the ectopic RFs result
from tangential interactions within striate cortex. However, we cannot
exclude the contribution of feedback connections from other cortical
areas, which are also exuberant during development (Price and
Blakemore, 1985) and thus could also mediate far-reaching interactions
between retinotopically noncorresponding loci.
The selectivity of tangential interactions
About three quarters of the ectopic fields had the same orientation
preference as the CRF. This suggests either that the remote input is
provided selectively and predominantly by cortical cells which have
the same orientation preference as the target cells, or that the remote
response is nonoriented and that orientation selective responses are
generated within the column, which contains the target cell. The authors
consider the latter possibility unlikely, because of the cases where the
orientation preferences of ectopic and classical RF did not match.
Rather, it appears that the ectopic inputs were derived from orientation
selective neurons. The implication is that the majority of the excitatory
long-range connections selectively couple cells with similar orientation
preference. This hypothesis is in agreement with observations of Maffei
and Fiorentini (1976) and Nelson and Frost (1985). These authors
reported facilitatory or disinhibitory effects from regions outside the
CRF which were strongest when the remote stimuli had the same
orientation as that preferred by the CRF. Further support for the
hypothesis of orientation matched input comes from three recent
observations. Firstly, the cross-correlation analysis of Ts'o et (11. (1986)
shows in adult cats selective excitatory coupling between cells with
similar orientation preference located in distant cortical columns.
Secondly, the investigation of stimulus dependent oscillatory responses
with multi-electrode arrays revealed that remote columns synchronize
their oscillatory activity if they have similar orientation preferences
and are activated with coherently moving stimuli (Gray er al., 1989).
Thirdly, a recent double labelling study by Gilbert and Wiesel (1989)
using 2-deoxyglucose autoradiography to visualize orientation columns
and injections of rhodamine-filled latex beads to label horizontal
intrinsic connections indicates that long-range lateral projections relate
columns of similar orientation specificity.
Another remarkable property of ectopic fields was that the majority
preferred stimuli moving toward the CRF. Such direction-selective
influences from outside the CRF have been reported previously (Fries
and Albus, 1973; Maffei and Fiorentini, 1976; Nelson and Frost, 1978;
Orban et al., 1987) and have been suggested to play an important role
in figure-ground discrimination or pre-attentive vision (see below).
Finally, the authors' results suggest selectivity of tangential interactions
with respect to ocular dominance also, as in 7 of 10 ectopic fields tested
for this property the eye dominance of the ectopic and the classical
RF was similar.
Functional implications
Our observations indicate that during early postnatal development,
neurons in kitten striate cortex receive excitatory input from areas in
the visual field more than 20" away from the location of the CRF,
suggesting that remote inputs might have a special function in integrating
information over several columns within the visual cortex. Selective
lateral excitatory connections between visual cortical neurons with
spatially separate, but otherwise similar RF properties have been
proposed as substrate for visual processes requiring a global analysis
of visual scenes, such as figure-ground discrimination (for review see
Allman et al., 1985; Julesz, 1984). Selective and co-operative
interactions between groups of cortical neurons coding for the same
features at different locations in the visual field have been suggested
as suitable mechanisms for the detection of coherencies in the feature
domain (Marr and Poggio, 1976; Poggio el al., 1985; Singer, 1987;
von der Malsburg and Schneider, 1986; von der Malsburg and Singer,
1988). The authors propose here that the ectopic fields reflect the
development of connections, which later serve such global scene
analysis. Specifically, the authors suggest that the appearance of ectopic
fields results from an initial exuberance of intracortical horizontal
connections, and that their later disappearance is the consequence of
a pruning process, which enhances the selectivity of coupling by
selectively stabilizing only those subsets of connections which link cells
that are frequently co-activated. Therefore widespread lateral
connections are probably not a transiently expressed epiphenomena
with no specific functional role, but more likely represent the necessary
substrate for the manifestation and experience-dependent modification
of these global aspects of information processing. The results described
in this and the two preceding studies are without exception compatible
with this interpretation. The anatomical data indicated a transient
376 Ectopic receptive fields in cat area 17
exuberance of intrinsic tangential connections, and the current sourcedensity analysis confirmed that excitatory interactions were stronger
and more far-reaching in kittens than in adult cats. Both phenomena
coincide in time with the occurrence of ectopic fields. T h e high
correlation between the R F properties of the ectopic and the classical
fields indicates preferential coupling between neurons with similar RF
properties. The finding that dark-rearing led to a reduction of tangential
connections beyond the normal level suggests that visual activity has
a stabilizing function. This, in turn, is compatible with the authors'
proposal that pruning of tangential connections occurs under the
influence of neuronal activity. The authors have n o direct evidence
for the hypothesis that those connections which link cells with correlated
activity patterns a r e stabilized selectively. However, such a process
has been shown t o occur during the development of other cortical
pathways, e.g. for the pruning and selective stabilization of binocular
connections (for review see Singer, 1985a. b , 1987; Stryker, 1982).
The finding that ectopic fields disappear in the adult suggests that the
persisting horizontal connections are not effective enough to generate
cell discharges by themselves. This, however, is not required if, as
demonstrated recently (Gray et al., 1989), coherent activation of remote
columns is expressed by the synchronization of their respective
oscillatory responses. In that case, tangential interactions must only
have a synchronizing effect, which can probably be assured with weak
interactions that by themselves d o not have to elicit cell discharges.
Acknowledgements
W e are most grateful to Helga Duckstein and Christa Ziegler for their
skillful technical assistance, to Gisela Knott and Gabricle TrautenLuhmann for excellent editorial support, and t o D r G. A . Orban for
his helpful comments on the results of this study. This report is part
of the P h D thesis of H . J . Luhmann, presented to the University of
Bremen.
Abbreviations
BIC
CRF
DDR
EEG
FET
GABA
GLU
NR
OD
PSTH
RF
SD
SE
TRF
bicuculline methiodide
conventional receptive field
dominant discharge region
electroencephalogram
field effect transistor
y-aminobutyric acid
glutamate
normally reared
ocular dominance
peristimulus-time histogram
receptive field
standard deviation
reared in selective environment
total receptive field
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