THE JOURNAL OF COMPARATIVE NEUROLOGY 276~1-29(1988)
Local Circuit Neurons of Macaque Monkey
Striate Cortex: 11. Neurons of
Laminae 5B and 6
JENNIFER S. LUND, MICHAEL J. HAWKEN, AND ANDREW J. PARKER
Department of Psychiatry, University of Pittsburgh, Pittsburgh, Pennsylvania 15261
(J.S.L.),
and Department of Physiology, Oxford University, Oxford, England (M.J.H.,
A.J.P.)
ABSTRACT
This study investigates the intrinsic organization of axons and dendrites
of aspinous, local circuit neurons of the macaque monkey visual striate
cortex. These investigations use Golgi Rapid preparations of cortical tissue
from monkeys aged 3 weeks postnatal to adult. We have earlier (Lund, ’87)
described local circuit neurons found within laminae 5A and 4C; this present
account is of neurons found in the infragranular laminae 5B and 6. Since
the majority of such neurons are GABAergic and therefore believed to be
inhibitory, their role in laminae 5B and 6, the principal sources of efferent
projections to subcortical regions, is of considerable importance. We find
laminae 5B and 6 to have in common at least one general class of local
circuit neuron-the “basket” neuron. However, a major difference is seen in
the axonal projections to the superficial layers made by these and other local
circuit neurons in the two laminae; lamina 5B has local circuit neurons with
principal rising axon projections to lamina 213A, areas whereas lamina 6
has local circuit neurons with principal rising axon projections to divisions
of 4C, 4A, and 3B. These local circuit neuron axon projections mimic the
different patterns of apical dendritic and recurrent axon projections of pyramidal neurons lying within laminae 5B and 6, which are linked together
by both dendritic and axonal arbors of local circuit neurons in their neuropils
extending between the two laminae. The border zone between 5B and 6 is a
specialized region with its own variety of horizontally oriented local circuit
neurons, and it also serves as a special focus for pericellular axon arrays
from a particular variety of local circuit neuron lying within lamina 6.
These pericellular axon “baskets” surround the somata and initial dendritic
segments of the largest pyramidal neurons of layer 6, which are known to
project both to cortical area MT (V5) and to the superior colliculus (Fries et
al., ’85). Many of the local circuit neurons of layer 5B send axon trunks into
the white matter, and we therefore, suspect them of providing efferent
projections. The axons of lamina 6 local circuit neurons have not been found
to make such clear-cut contributions to the white matter.
Key words: vision, inhibition, interneuron, visual cortex, primate
This study continues a morphological description of the
organization of local circuit neurons with smooth or sparsely
spined dendrites in the monkey primary visual cortex
(Lund, ’87). The local circuit neurons are believed to be
responsible for inhibitory or modulatory control of the excitatory neurons in the cerebral cortex-the pyramidal neurons and stellate neurons-which retain marked dendritic
0 1988 ALAN R. LISS, INC.
spine populations into maturity (Lund, ‘73). A recent study
on the population of neurons within striate cortex that
contain the inhibitory transmitter substance y-aminobutyric acid (GABA) or its synthetic enzyme glutamic acid
Accepted April 6, 1988.
J.S. LUND ET AL.
2
decarboxylase (GAD) shows layers 5 and 6 neuron populations each to contain about 12% of GABA or GAD positive
neurons (Fitzpatrick et al., '87). This is quite comparable to
their density in laminae covered in our earlier study of
interneuron organization (laminae 4Cp about 14%,and 4Ca
about 15%).Since lamina 4C/3 has almost twice the cell
density of 5B, the density of GABAergk neurons may be
more a reflection of the total number of neurons in a particular lamina than being determined on some other basis.
Crucial data on the precise number of particular kinds of
local circuit neuron are, however, largely lacking, except
for the relatively sparse number (less than 10%)that can
be identified by the colocalization of various peptides Mendry et al., '83, '84; Jones and Hendry, '85, '86). There is
some concern even here, however, that numbers of neurons
obtained by using antibody labels may be minimum figures
since activity level determines whether or not the label
appears significant to the human eye-and activity level
may vary from cell to cell (see, for instance, Hendry and
Jones, '86).
It is clear that single pyramidal neurons may receive
input from the axons of several different varieties of interneuron. For instance, there are chandelier neurons (Somogyi, '77; Fairen and Valverde, '80) that target pyramidal
neuron initial axon segments; "basket" cells that target
the somata and initial dendritic segments (Freund et al.,
'831, and other local circuit neurons seem to show a preference for the more distal dendritic segments (Somogyi and
Cowey, '81, '84); in addition, the apical dendrite can pass to
other laminae where different local circuit neurons may
contact its surface compared to the basal dendritic field. We
have, therefore, examined laminae 5B and 6 for interneuron classes that might target different regions of the pyramidal neurons within these laminae.
The comparison of local circuit neuron populations in
laminae 5B and 6 also involved us in the question of to
what degree layers 5B and 6 interact with each other and
how the local circuit neurons might participate in that
interaction. Another question also arose: whether particular functional sublaminar zones exist in layers 5B and 6,
which might be the targets of specific populations of interneurons. We also looked for interlaminar projections by the
local circuit neurons in laminae 5B and 6 to more superficial layers. We were interested to see whether the neurons
of 5B and 6 participate differently in these projections (since
interlaminar axon projections by local circuit neurons had
proved to be extensive and very specific in our earlier studies of local circuit neurons in laminae 4C and 5A; Lund,
'87).
The different functional roles of laminae 5B and 6 suggested that we might find differencesbetween them in their
populations of interneurons. It is known, for instance, in
the monkey that layer 6 neurons show direction specificity
to moving targets, whereas layer 5 neurons do not (Livingstone and Hubel, '84; Hawken et al., '88). It is also known
that layers 5B and 6 differ markedly from each other in the
external targets of their populations of efferent neurons
(Lund et al., '75; Fries et al., '85; Kennedy and Bullier, '85),
in the projections they receive from the other more superficial layers of cortex (Blasdel et al., '85; Fitzpatrick et al.,
'85), and in afTerents from other cortical and subcortical
regions (Hendrickson et al., '78; Van Essen, '84)--factors
that might also be reflected in different organization of
interneurons within their neuropils.
Our first study in this series (Lund, '87) offered an explanation for why we are using Golgi impregnations for these
studies when, in theory, intracellular filling with horseradish peroxidase or other tracer would provide a fuller image
of the neuron. As noted, the excessive number of primates
needed and the labor of such intracellular filling are currently significant obstacles to such studies. For these reasons the Golgi impregnations of infant monkey striate
cortex (where myelination has not yet blocked axonal impregnation) here provides material for at least the beginnings of a detailed study of the organization of these
important neurons.
Short reports of some aspects of this work have appeared
earlier (Lund et al., '87a,b).
MATERIALS AND METHODS
These are reported in full in Lund ('87) and are not repeated at length here. Golgi Rapid impregnations, cut a t
90 pm from blocks of infant Macaca nemestrina and M.
fascicularis monkeys, were used. The processes of individual neurons were often traced through a number of consecutive sections and Figure 1A-D in Lund, '87 illustrate the
laminar numbering system for monkey cortex used in the
following description. The neurons are grouped in terms of
varieties which are classified first in terms of the lamina in
which the soma customarily lies, and then a number that
implies nothing more than the investigators' order of description of neurons in that lamina. The term class is used
to identify neurons that are suggested to have a common
physiological action by virtue of their anatomical form and
other information gathered about such cells. For instance,
the neurons of "chandelier" morphology (Somogyi, '77)
would form a class (see Lund, '87 for a more detailed discussion of these terms).
RESULTS
Local circuit neurons of lamina 5B
It is clear from our studies of local circuit neuron morphology in striate cortex that dendritic morphology can
rarely, if ever, be used as a defining characteristic of neuron
variety or class. It is the quality and pattern of distribution
of the axon that most clearly provides an identity to the
neurons we describe below.
Variety 5B-1
The neurons of variety 5B-1 (Figs. lb, 2b) have cell body
and dendrites confined to lamina 5B with a roughly radial
dendritic spread of 250-300 pm lateral extent. The axon
arises on the pial side of the soma and stout horizontal
trunks emerge from this rising axon within lamina 5B and
spread laterally about 450 pm from the soma within 5B,
giving a lateral spread of a t least 800-900 pm to the local
axon arbor in 5B. The terminal beaded collaterals of the
axon arbor are somewhat more dense in the vicinity of the
dendritic field and largely omit lamina 5A in their distribution. The stout rising axon trunk reaches lamina 3A
without forming collaterals, then rapidly divides into a
number of branches, forming a dense, laterally confined
(200-300 pm) terminal arbor within 3A and 2. A fine descending axon process enters lamina 6 and may enter the
white matter without contributing significantly to lamina
6. The general form of the axon arbor within 5B suggests
this neuron may belong to the "basket" neuron class
(Freund et al., '83).
Variety 5B-2
The variety 5B-2 neurons (Figs. la, 2a) have a similar
dendritic arbor t o variety 5B-1. Their dense local axon arbor
2
LOCAL CIRCUIT NEURONS OF MONKEY VISUAL CORTEX
1
3
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[a]
3A
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3B
3B
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Fig. 1. (a) Local circuit neuron of the 5B-2 variety. The axon characteristics are a dense local arbor, not much wider in lateral extent than the
dendritic field, within lamina 5B and a stout axon trunk that rises to the
superficial laminae giving a sparse arbor in 4N3B and a profuse arbor in
the 2/3A region. The 5B-2 variety usually has descending axon trunks that
enter the white matter with only a few weak collaterals in lamina 6.
(Another example of this variety is seen in Fig. 2a.) (b)Local circuit neuron
of the variety 5B-1. The axon characteristics are a wide-spreading axon,
6
perhaps of the “basket” axon type, within lamina 5B and a rising axon
trunk ascending unbranched until a rather laterally restricted terminal
arbor in lamina 213A. The dendrites of these neurons appear very similar
in form and extent to the 5B-2 variety (see Figs. l a , 2a). (Another example
of the axon arbor of the 5B-1variety is shown in Fig. 2b.) Both (a) and CO)
are from Golgi Rapid impregnations of 3-week-oldMucacu nernestrinu. Scale
bar = 100 gm.
J.S. LUND ET AL.
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3A
4
3B
4A
4A
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4B
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axon
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Figure 2
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LOCAL CIRCUIT NEURONS OF MONKEY VISUAL CORTEX
is formed from branches that emerge from the stout axon
trunk shortly after it leaves from the pial side of the soma.
The local axon within 5B differs from that of the 5B-1
variety in that it barely exceeds the width of the dendritic
arbor (about 300 pm in lateral spread) and the beaded
collaterals are somewhat finer and denser in their arbor.
The rising axon trunk reaches lamina 4A before sparse t o
moderate numbers of collaterals emerge, but the main superficial arbor occurs in lamina 3A and 2. The width of this
arbor may match or exceed the arbor in 5B. Occasional
cells occur where the soma lies high in lamina 5, but the
dendrites still bridge the width of the lamina 5 division;
the local axon arbor favors the upper half of 5 and the
rising axon trunk begins its terminal arbor somewhat lower,
in upper lamina 3B. The 5B-2 neurons have one or two
descending axon trunks that pass down through lamina 6,
where they give off a few fine collaterals, then pass into the
white matter.
Variety 5B-3
Variety 5B-3 (Fig. 3) is of the chandelier class and typically the soma lies near the base of 5B on the border with
lamina 6. The dendrites characteristically bear forked distal tips and may either reach up through the whole depth
of lamina 5B or may not reach the upper border; the dendrites do, however, generally bridge the 5-6 border. The
axon emerges from the white matter aspect of the soma and
spreads locally at the 5-6 border and upward to the base of
lamina 5A, having a lateral spread of 200-250 pm. Whereas
the processes of this neuron variety intrude into upper
lamina 6, both axon and dendrites are biased in their distribution to lamina 5B and this class of cells has not yet
been found with soma well into lamina 6, so these cells are
here designated a variety of lamina 5B.
Variety 5B-4
Variety 5B-4 are local circuit neurons (Figs. 4b, 5) of
lamina 5B that lack a rising axon trunk with arbor in the
superficial layers. Their dendrites bridge the depth of 5B
spreading laterally about 250 pm. Their axon can form a
local arbor, within and little wider than the dendritic arbor
(approximately 300 pm; Fig. 4b) or, if the soma lies near the
base of 5B, the axon may favor the 5-6 border region with
somewhat wider lateral extent (500-600 pm) and show not
much overlap with the dendritic field (Fig. 5). These neurons have descending axon trunks that enter the white
matter without substantial contribution to layer 6.
Variety 5B-5
The 5B-5 variety of neuron (Fig. 6) is large compared to
the other local circuit neurons of 5B, the soma measuring
close to 20 pm in diameter and the dendrites spreading
350-400 pm in total lateral extent. The dendrites reach the
upper margin of lamina 5 and may either extend down to
Fig. 2. (a) Local circuit neuron of the 5B-2 variety. The characteristic
feature is the stout axon trunk rising t o the superficial layers with sparse
collaterals in the 4N3B region and a profuse arbor in 2/3A. The local axon
arbor in 5B is profuse but not much wider than the dendritic arbor in lateral
extent. Descending axon trunks pass to the white matter with sparse collaterals in lamina 6. (Another example is seen in Fig. la.) 0)The axon of a
local circuit neuron of the 5B-1 variety. The dendrites and soma were not
impregnated; the axon initial segment is indicated with an asterisk. The
confined dense terminal arbor in 2/3A and the spreading axon arbor in 5B
is typical of this variety. (Another example is seen in Fig. lb.) Both neurons
(a) and 03) are Golgi Rapid impregnations from 3-week-old Mucaca nemestrina. Scale bar = 100 p m .
5
the white matter or intrude only into the upper portion of
layer 6. The axon that arises on the pial surface of the soma
forms a cone-shaped descending arbor that includes both
layers 5 and 6, widening its lateral extent (500-600 pm) as
it spreads downward. The main axon trunks are stout and
their beaded terminal collaterals have characteristics vertical and obliquely angled trajectories within laminae 5B
and 6. A rising axon trunk reaches at least to upper 4Ca
without branching, but so far its final target has not been
identified-the impregnation ceasing within the section,
probably as a result of early myelination. This variety of
neuron does not clearly contribute axon trunks to the white
matter.
Comments on local circuit neurons of 5B
As we endeavor to provide a description of neurons in the
5B region, it can sometimes be questioned whether neurons
belong to the 5A region or are properly considered part of
the 5B population (see Lund, ’87 for a description of the 5A
local circuit neurons). Figure 4a shows a neuron that probably belongs to the 5A region, although we did not describe
a cell of quite this kind in our earlier study. Although the
soma lies a little lower than the base of 5A, its dendritic
field and axon arbors (predominantly in 5A and lamina 6)
resemble those of variety 5A-2. The rising axon arbor resembles those of the 6-6,type (i)variety to be described that
have fine diameter rising axons with collaterals in 5A, mid
to upper 4C and in 4A. We suggest that this neuron be
classed as a variety 5A-2 neuron, and thus we broaden the
5-2 variety to include neurons that have rising axon projections to upper 4C& 4Ca, and 4A (5A-2i) as well as those
with axon arbors targeting only 4Ca (5A-2ii)as described
in Lund (‘87).
Cells of the 5-6 border region: Variety 5B:6-1
There is indication from the distribution of axons and
dendrites of several varieties of local circuit neurons of
laminae 5B and 6 that the zone where laminae 5 and 6
meet is a specialized region. There is, moreover, one group
of local circuit neurons that largely restricts its dendritic
and axonal process to this region. Variety 5B:6-1 (Fig. 7)
has long, horizontally oriented dendrites that reach up to
250 pm from the soma-giving a lateral spread of 400-500
pm to the dendritic field. The axon, which generally arises
from the white matter side or a lateral pole of the soma,
forms stout laterally spreading trunks with short, rather
sparse beaded terminal collaterals that tend to have vertical trajectories. The axon trunks can reach at least 400 pm
from the soma, giving a potential total spread of 800-900
pm, with a narrow depth to the axon field of approximately
150 pm. Whereas a three-dimensional analysis has not been
carried out on these neurons, their processes do not seem to
evenly cover a circular territory around the soma, but may
have a particular trajectory relative to the overall pattern
of the neuropil. The general form of the axons of these
neurons suggests they belong to the “basket” neuron class.
Local circuit neurons of lamina 6
The local circuit neurons of lamina 6 present some particular difficulties for classification.Many of the neurons have
dendrites that extend to the top of lamina 5B; either just
one or two of their dendrites can stretch this distance, with
the bulk of the arbor in lamina 6, or the dendrites may be
evenly distributed to both layers 5 and 6. This raises the
question whether this variable dendritic extension consti-
b
5B
b
6
Fig. 3. Two examples of neuron variety 5B-3. The axons for each cell
have been drawn separately and displaced laterally for clarity. This variety
is of the chandelier class and characteristically the soma lies on the 5-6
border with dendrites largely ascending into lamina 5B. Note the forked
tips of the dendrites and compare with the similar dendritic form of neurons
of variety 6-2 seen in Figures 10a and llb. The axon arises from the aide or
white matter pole of the soma and has its principal arbor within 5B and
along the 6-5B border. Both cells are from Golgi Rapid impregnations of
tissue from 3-week-oldMacaca nemestrina. Scale bar = 50 pm.
4A
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Fig. 4. (a) This neuron is believed to belong to the group called variety
5A-2 (see Fig. 10 of Lund, '87, and text of that account). These neurons
emphasize a dendritic arbor in 5A and descending dendritic branches that
reach to the base of lamina 6. The axon distributes in 5A and in a descending cascade that has most collaterals within lamina 6. The axons of the cell
illustrated here resembles those of our earlier described 5A-2 neurons in
arborizing in divisions of lamina 4; but here the axon seems to contribute
to upper 4C@,4Ca, 4A,and lowermost 3, rather than just in 4Ca, a s our
previous examples had shown. In its rather wide axon distribution, the 5A2 example shown here resembles some of the 6-6, type (i),neurons; (see Figs.
4
17, 19a). whereas the earlier 5A-2 examples had rising axons arborizing in
lamina 4Ca resembling other 6-6neurons-here called type (iiMsee Figs.
18, 19a, 20). These similarities in axon distribution between the 5A-2 and
6-6 varieties are believed to illustrate parts of circuits that closely link
laminae 6, 5A, divisions of 4C, and 4Mower 3B. (b) This neuron is of the
5B-4 variety, which lacks projections to the superficial layers. The axon is
profuse and localized close to the dendritic field in 5B. Descending axon
trunks pass to the white. matter without contributing to lamina 6. (Another
example of a 5B-4 neuron is shown in Fig. 5.) Both cells are from Golgi
Rapid impregnations of 3-week-old Macaca nernestrina Scale bar = 100 pm.
J.S. LUND ET AL.
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4
6
Fig. 5. An example of a 5B-4 neuron whose axon shows less overlap with
its dendritic field than in the example shown in Fig. 4b. Here the dendrites
bridge the depth of lamina 5 and the soma lies on the 5B/6 boundary. The
axon spreads broadly in lower 5B largely beyond the range of the dendrites.
tutes a sufficient reason for forming varietal subcategories
or if one simply accepts that occasional dendrites of the
local circuit neurons of lamina 6 escape a developmental
constraint on their dendritic processes to keep their arbor
below the upper boundary of layer 6. We have chosen the
latter viewpoint when the bulk of the dendrites lie in layer
6. When the dendrites commonly distribute evenly between
layers 5 and 6, we find this grounds for consideringwhether
or not these neurons are a distinct variety.
Variety 6-1
The 6-1 neurons (Figs. 8, 9) are large, with a substantial
spreading field of dendrites extending largely below the
soma that lies in mid to lower lamina 6. The dendrites,
which reach up to 400 pm from the soma, can travel well
into the white matter. An occasional single dendrite may
deviate from the main arbor and pass vertically to the top
of lamina 5. The axon arises on the pial side of the soma
and gives off stout trunks that travel long distances (at
least 500 pm from the soma) within layer 6 with some
intrusions into lower layer 5B. An occasional fine axon
collateral may travel with an excentric dendrite to reach
the top of layer 5, but these neurons do not appear to
contribute axon arbors to regions above lamina 5. The
rather infrequent beaded axon collaterals that emerge from
the stout laterally traveling trunks often have a somewhat
vertical trajectory. The form of these axons suggests that
these neurons belong to the “basket” neuron class.
There is no rising axon trunk, but a descending trunk reaches into the
white matter. Golgi Rapid impregnation from 3-week-old Macaca nemest r i m monkey. Scale bar = 50 pm.
Variety 6-2
The dendrites of 6-2 neurons (Figs. 10, llb) are confined
to lamina 6, and they spread largely below the soma that
lies near the upper margin of layer 6. Their dendrites follow
a rather tortuous downward course establishing an arbor
250-300 pm wide, and they often end in a forked tip, much
as do the dendrites of the chandelier class neurons of variety 5B-3. The axon arises apically and, local to the cell’s
dendritic field, provides a cascade of stout branches that
break into terminal collaterals with exceptionally large
diameter terminal “beads.” Stout axon trunks also pass
laterally considerable distances from the cell body (at least
500 pm from the soma) and emit clusters of beaded collaterals that can closely wrap around the somata and initial
dendritic segments of large neurons of pyramidal form (visible in the tissue background by virtue of a slightly darker
Fig. 6. Two examples of the variety 5B-5 local circuit neurons. The
dendrites may intrude only slightly into lamina 6 (e.g., example (a) from
the perimacular representation) or they may reach from the upper boundary
of 5 down to the white matter (e.g., example (b)from the peripheral field
representation in the roof of the calcarine fissure). The axon forms a characteristic cascade of descending branches occupying both lamina 5 and 6
with collaterals that emphasize oblique and vertical orientations. A vertically rising axon trunk is present (see segments marked with asterisks in
(a) and (b)),but so far this rising, unbranched axon process has not been
traced beyond upper 4Ca, ceasing to impregnate within the section, probably due to myelination. Golgi Rapid impregnations from 3-week-oldMacaca
nemestrina. Scale bar = 50 um.
LOCAL CIRCUIT NEURONS OF MONKEY VISUAL CORTEX
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Figure 6
J.S. LUND ET AL.
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Fig. 8. This figure and figure 9 are two examples of local circuit neuron
variety 6-1.The cell bodies of these cells lie in mid to lower 6 with a
dendritic field that spreads widely down through lower lamina 6 and into
the white matter; an occasional dendritic process may reach into lamina 5.
5
The axon is robust, like the spreading dendritic field, and stout trunks
travel laterally away from the cell with prominantly beaded collaterals.
Their form suggests they belong to the “basket” neuron class. Golgi Rapid
impregnations from 3-week-old Macacu nernesh-ha. Scale bar = 100 gm.
5
c c
6
m
P*
J.S. LUND ET AL.
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5
5
6
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Fig. 9. A further example of a neuron of the 6-1 class; see Fig. 8 and legend for description. Golgi Rapid
impregnation from 3-week-oldMacaca nemestrina. Scale bar = 50 pm.
than background stain in the cytoplasm),lying usually but
not always high in the layer near the 5-6 border. These
pericellular arrays, truly “baskets” of terminals, are often
also found along this border without a traceable connection
to a cell of origin and it appears that the large diameter
collateral trunks are already myelinating by 2-3 weeks
postnatal. A stout rising axon trunk can usually be found
emerging from the initial axon segment, but so far the
destination of this rising axon has not been traceable, the
trunks ceasing to impregnate within the section in lamina
5-again probably due to early myelination.
aspect of the soma is of large diameter with prominent
terminal beaded collaterals; stout trunks spread laterally,
especially near the 5-6 border, which they may cross to
enter lamina 5B to a limited extent. The total width of the
axon arbor is 450-600 pm (which may reach its greatest
width for neurons of the calcarine roof, i.e., peripheral field
representation; Fig. 12). If the cell has any dendritic processes extending vertically into lamina 5, a small number
of axon collaterals may travel with them to reach the upper
margin of lamina 5. This neuron variety may be of the
“basket” class.
Variety 6-3
Variety 6-4
The 6-3 variety (Figs. lla, 12, 13) of local circuit neuron
has a robust dendritic field in lamina 6 with a 350-400 pm
width at the upper margin of the layer and a narrower field
of descending dendrites that reach and enter the white
matter. An occasional single dendrite may extend vertically
into lamina 5. The axon that arises on the pial or lateral
The 6-4 variety (Figs. 14, 15)may comprise several different cell types, but we cannot yet be confident of an accurate
description of each, so we grouped them as a single 6-4
variety. In general these cells have a narrow (150 pm)
vertically extended bitufted (double bouquet) form of dendritic field with a prominent bunch of dendrites reaching
Fig. 10. (a) The 6-2 local circuit neuron variety has its soma in upper
lamina 6 and a descending array of rather tortuous dendrites, many of
which end with forked tips, like the earlier illustrated chandelier neurons
(see Fig. 3). These neurons have very prominently beaded axons, which
form an arbor local to the dendrites as well as stout trunks that travel for
long distances laterally, particularly in upper lamina 6. Pericellular clusters of terminals are given off from these trunks and oRen the cell bodies
and initial dendritic segments of large pyramidal neurons can be seen as
dark shadows within these terminal clusters. Often the pericellular clusters
occur in isolation, emerging from portions of the stout trunks, and it is
probable that the axon trunks are already myelinated in the early postnatal
period, making it difficult to trace the connections between cell and terminal axon arrays. In (b) several isolated pericellular clusters are drawn for
comparison. These 6-2 neurons also appear to have rising axon trunks (see
asterisk in (a)),but these have ceased to impregnate within lamina 5 in
material examined so far. (Another example is seen in Fig. llb). Golgi
Rapid impregnations from 3-week-old Macaca nernestrina Scale bar
= 50 Cm.
5
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Fig. 11. (a) This neuron and those of Figs. 12 and 13belong to the variety
6-3. These neurons have well-developed dendritic fields in lamina 6, which
widen in lateral extent near the top of lamina 6. An occasional dendrite
may extend into lamina 5. The axon is of large diameter with prominent
beaded terminal collaterals that again spread most widely in upper lamina
6. (b) This neuron is of the 6-2 variety (see also Fig. 10) and shows the
charadenstic forked tips at the ends of its dendrites. Whereas this cell did
1 %
5
to their terminal
not havelaterally spreading trunks that could be followed
f
collaterals, the local axon enclosed a large cell soma lying lower in layer 6
amongst a tangle of the cell’s dendrites. The rising axon trunk ceased to
impregnate within the section thickness (see asterisk) as has been found
typical of this cell type in our material. Both cells are from Golgi Rapid
impregnations in 3-week-oldM w w a nemestrina. Scale bar = 50 pm.
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Fig. 12. An example of the 6-3 variety of neuron from the roof of the
calcarine fissure (i.e., peripheral field representation). The dendrites and
axon6 of these neurons may reach their maximum lateral spread, paxticu-
lady at the 5/6 border when lying in the calcarine fissure. (See Figs, Ila
and 13 for other examples.) Golgi Rapid impregnation from 3-week-old
Macaca nernestrina. Scale bar = 50 pm.
J.S. LUM) ET AL.
4
6
b
Fig. 13. A further example of a 6-3variety of neuron. (See Figs. l l a and 12 for other cells of this variety.) Golgi
Rapid impregnation from 3-week-oldMuceca nernestrina. Scale bar = 50 pm.
diameter; some (see, for instance, Figs. 18, 19a) are robust,
with large diameter, beaded terminal collaterals, whereas
others are exceptionally fine and difficult to follow (Figs.
17,20a. In terms of distribution, whereas their axon arbors
can include upper 4Cp and 5A, the lower 4Cp region between these two divisions seems t o be omitted, as is layer
4B, and no arbors have been traced above lowermost lamina 3B. In general, neurons whose axons that provide collaterals to mid 4C (upper 4Cp and lower 4Ca; Figs. 17,19b)
also have collaterals in 5A and may add a terminal arbor
in the 4A region; their diameter is generally fine; we have
called this type 6). The axons that favor 4Ca, in particular
upper 4Ca, seem of larger diameter and although occasional collaterals are seen in 5A, collaterals in this region
Variety 6-5
are not prominent (Figs. 18, 19a, 20); we have called these
These 6-5 cells (Fig. 16)strongly resemble the 5-5 variety neurons type (ii). The axon arbors in lamina 6 of the neuin axon form, although their dendritic arbor is narrower rons with rising projections to 4Ca often (but not always)
(250-300 pm) and emphasizes a distribution in layer 6. The resemble those of the “basket” axon class.
axon forms a cascade of vertical and oblique collaterals in
both laminae 5B and layer 6 and has a lateral spread of a t
Comments on local circuit neurons of 6
least 500 pm. It is uncertain if this 6-5 variety ever contribAttention was paid to neurons lying below layer 6 in the
utes any axon processes to layers above lamina 5.
white matter. In general their axons were hard to follow
Variety 6-6
and incomplete. However, we feel that those neurons we
The 6-6 variety (Figs. 17-20)certainly contains different have so far found in our tissue, whose somata and dendrites
cell types, but for the present they are grouped together in lay mainly within the white matter, are not of a special
terms of their common feature of providing rising axon class or single morphology. Rather, they appear to resemble
projections to one or more of the laminae closely associated the varieties we have already already illustrated and seem
with thalamic inputsAC, 4A, 5A-as well as having a local to have been somewhat distorted by their position with the
axon arbor within lamina 6. Most but not all have two or predominantly horizontally oriented fiber layer.
more long vertically oriented dendrites that regularly reach
DISCUSSION
the top of 4Ca and even extend as far as 4A; they also have
a more numerous set of shorter basal dendrites that reach
It is clear from this examination of the local circuit neudown to the white matter. The axons of the cells of this rons of laminae 5B and 6 that classes that have been degroup can differ significantly from one another in their scribed previously in cerebral cortex, e.g., “basket” neurons
the upper border of lamina 5 as well as descending dendrites reaching the white matter (Figs. 14a-c, 15). The axon
differs in character from that of the 6-3 variety, being of
finer diameter and having smaller terminal boutons; it
forms a dense local field in layer 6, a little wider than the
dendritic field (250-300 pm); a slender rising axon process
provides minimal input to layer 5. Figures 14c and 15 show
two deviations from this typical form: Figure 15 shows a
neuron with a somewhat wider spread of axon and dendrites within layer 6, and Figure 14c illustrates a neuron
with an axon that favors the 5-6 border zone rather than
being largely confined to layer 6. For the moment we place
these neurons in the 6-4 group.
5
b
la1
A
b
5
b
Ibl
Fig. 14. Parts (a) and (b) show typical examples of local circuit neuron
variety 64. The bitufted dendritic field spreads equally into laminae 5 and
6, whereas the axon forms a prolific local field within layer 6 with only
minimal input to layer 5. Part (c)shows one variation in the 6 4 form where
x
d
the axon arbor favors the 5-6 border region in its terminal field rather than
being confined largely to layer 6. (See another example in Fig. 15.) All are
Golgi Rapid impregnations from 3-week-old Mucucu nemestrinu. Scale bar
= 50 pm.
6
5
b
J.S. LUND ET AL.
18
v
m
m
i
A
i
5
Fig. 16. This neuron is of the 6-5variety. The axon and dendrites have
been drawn separately for clarity. Note the strong resemblance of the axon
to that of the 5-5variety (see Fig. 6). Whereas the dendrites are largely
confined to lamina 6, the axon forms a cascade of vertical and oblique
branches in both 5B and 6. We have not yet found a clear axon contribution
to more superficial layers from this cell type. Golgi Rapid impregnation
from 3-week-oldMacaca nernesh-ina. Scale bar = 50 pm.
6
5
x
M
0
0
J.S. LUND ET AL.
20
4B
4
4Ca
5
6
Figure 17
LOCAL CIRCUIT NEURONS OF MONKEY VISUAL CORTEX
(Freund et al., ’831, “chandelier” neurons (Somogyi, ‘77),
“pericellular basket” neurons (“nib pericellu1aires”Ramon y Cajal, ’11; Marin-Padilla, ’69; Martin et al., ’83),
and double bouquet or bitufted neurons (Somogyi and
Cowey, ’ 8 l t a r e all present in these layers, together with
neurons that have not yet been given descriptive class
names. We must admit to being generous with the term
basket neuron and therefore with the implication that the
axons of such cells prefer to contact the cell body and
proximal dendritic segments of pyramidal neurons (Freund
et al., ’83;Martin et al., ’83). Of course, we have no evidence
here of such a contact preference or that cells we have said
resemble basket neurons are indeed of a common class.
An important issue is whether the axonal and dendritic
processes of these various local circuit neurons do indeed
recognize laminar or sublaminar boundaries in cortical
depth, i.e., can be broken down as we have suggested into
varietal laminar subgroups. A parcellation of territory
would suggest that the neurons are particularly concerned
with functional events occurring within particular spatial
limits in the cortical neuropil. Since we know that the
physiological response properties of neurons in laminae 5B
and 6 differ (Hubel and Wiesel, ’68; Livingstone and Hubel,
’84;Orban et al., ’86; Hawken et al., ’87), restriction of the
processes of individual neurons to one or other of these
territories suggests that they might be part of the substrate
for generating the particular response properties seen in
each laminar division. From the preceding description of
local circuit neurons, we believe it to be clearly illustrated
that laminae 5B and 6 have their own populations of local
circuit neurons. Whereas neurons of the same class can
occur in both laminae, comparing the varieties of the same
class present in laminae 5B and 6, they are found to have
distinct differences in their interlaminar axonal projections
and should therefore differ in the functional outcome of
their activity in terms of visual processing within area VI.
Only one cell class-to which the varieties 5B-5 and 6-5
both appear to belong-has an axon projection from single
neurons that includes within signifkant portions of its arbor both laminae 5B and 6; but even for these neurons it is
clear that their dendrites do not always sample the 5B and
6 laminae equally.
Whereas the dendritic and axonal fields of all but one
variety (5B:6-1) of the 5B and 6 local circuit neurons bridge
the depth of at least their primary lamina, the lateral
extent of their axon and dendrites within the lamina varies
considerably between different varieties. In this regard, it
is found that lateral dendritic spread of individual neurons
is not a reliable indicator of the extent of their axonal
spread; for instance, the pericellular “basket” neurons (variety 6-2)have quite narrow dendritic fields but very extensive lateral spread of their axons. Another example is the
5B-1 variety, which has much the same dendritic spread as
the 5B-2 variety, but the axon spread of the former far
outreaches in lateral extent that of the latter. It is possible
21
that the dimensions of axonal spreads we see in the G l g i
material are relatively accurate and relate to other aspects
of the scaling of events in the striate cortex. For instance,
the largest “basket” cells have axonal spreads in the order
of 800-1000 pm; this distance is close to the sum of 2 ocular
dominance column widths (i.e., a right eye-left eye doublet
or a distance that enables columns of the same ocular
dominance to interact). A second order of magnitude seen
commonly for axon spread is around 450-500 pm, which
would be closer to a single ocular dominance column width
or perhaps linking a right eye-left eye pair. The narrowest
axonal spread (200-250 Fm) seems to be that of the chandelier neurons of lamina 5B (variety 5-3). The different
scale of axon spread between the basket neurons and chandelier neurons, both of which are supposed to exert inhibitory control on pyramidal neurons (the chandelier axons
contacting axon initial segments and the basket neurons
contacting cell body and dendritic initial segments), suggests a quite different lateral scale of relationship between
each class and the postynaptic pyramidal neuron populations. Each chandelier neuron would presumably control a
small closely adjacent group of neurons, whereas the basket
neurons would each contribute to the control of a rather
widely scattered group of postsynaptic neurons.
The extent of the local circuit neuron axon arbors should
be seen much better in neurons that have been well filled
intracellularly in vivo with HFtP. It will be interesting to
see if a reasonable sample of such data for these local circuit
neuron populations can be generated, but for the moment
we can accept the Golgi data only as providing minimal
estimates of axon spread. Another question, also probably
best answered in HRP filling studies, is whether over longer
distances specifically orientated trajectories or clustering of
terminals occurs in the local circuit neuron axon fields
(Martin et al., ’83; DeFelipe et al., ’86), features that have
been demonstrated particularly clearly in pyramidal neuron axon projections (Gilbert and Wiesel, ’83; Martin and
Whitteridge, ’84).
Local circuit neurons of lamina 5B
The local circuit neurons of 5B (see Fig. 21) include in
their axon targets projections to the superficial layers, with
an emphasis on terminals in the 3A-2 laminar division. It
is already known that pyramidal neurons of layer 5B have
recurrent axon projections to the 3A-2 region (Lund and
Boothe, ’75) and small injections of HRP into lamina 5B
show the strongest axonal projection from the layer to be to
the same 3A-2 division of the superficial layers (Blasdel et
al., ’85). In regard to retrograde labeling, injections of HRP
made in the 3A-2 laminar division result in heavy cell body
labeling in lamina 5B, whereas injections into the 3B-4A
division give most retrogradely labeled neurons in lamina
5A. A similar pattern is seen with injections of [3H] GABA
into the upper layers (Somogyi et al., ’83).We have seen in
our first study of local circuit neurons (Lund, ’87)that the
5A local circuit neurons do not emphasize a projection to
the 3A-2 division but have either an even distribution
Fig. 17. This neuron and that shown in Fig. 19b are of the variety 6-6, through the superficial layers including layer 1, or more
type (i). The 6-6 variety is distinguished by having axon projections to one prominently emphasize projections to 3B and 1. The coincior more divisions of 4C, and sometimes the arbor includes 4A, lowermost
3B, and 5A. The type (i) illustratedhere has a fine caliber axon that includes dences in projection patterns of pyramidal and local circuit
in its terminal distribution laminae 5A, upper 4C0, and lower 4Ca. The neuron projections for neurons in 5B and 5A, and the differtype (i) 6-6neuron shown in Figure 19b illustrates the finding that the axon ence in relationship between the 5A and 5B laminae and
of this variety also may include the 4M3B region in its arbor. The dendrites the upper and lower regions of the superficial zone of the
of the 6-6 neurons form a bitufted array with the upper tuR reaching as far
as the terminal axon array (i.e., well into 4C or even to 4A). Golgi Rapid cortex, indicate a clear lockstep relationship of inhibitory
and excitatory circuits. Physiological differences between
impregnation from 3-week-old Macaca nernestrina. Scale bar = 100 pm.
J.S. LUND ET AL.
22
4
4Ca
4ca
4cP
5
4
5
4
Fig. 18. The neuron illustrated belongs to the 6-6 variety and is of type
(ii). The axon projection to upper 4Ca is robust as are the local collaterals
in lamina 6. This neuron lies in the roof of the calcarine fissure. The axon
projection to 4Ca is the particular feature of the 6-6, type (ii) neurons, and
a robust spreading arbor in lamina 6 is seen in many type (ii) cells. (See
6
4
also Fig. 19a, and two neurons with axons of finer caliber projecting to
4Ca-also placed in the 6-6 type (ii) group-are shown in Fig. 20). &lgi
Rapid impregnation from 3-week-old Mucaca nemestrina. Scale bar = 50
pm.
LOCAL CIRCUIT NEURONS OF MONKEY VISUAL CORTEX
23
4A
4
4B
b
4Ca
4Ca
4
4cP
4cP
4
b
5
5
4
4
Fig. 19. (a) An example of a variety 6-6 neuron of type (ii) where the =On
projects to 4Ca and has a robust spreading arbor in lamina 6. The asterisk
marks an axon trunk that failed to impregnate, whereas the other branch
of the same rising axon was traceable to an incomplete arbor in 4Ca.
(Another,more complete example of this cell type is shown in Fig. 18.)@) A
6
1
t
6-6 neuron of type (i). This neuron has fine caliber axon projections to 5A,
upper 4CD, 4Ca, and the 4M3B region, as well as an arbor within lamina 6.
(Another example is shown in Fig. 17.) Golgi Rapid impregnations from 3week-old Mmmu nemestrina. Scale bar = 100 fim.
J.S. LUND ET AL.
24
4Ca
b
4cP
5
5
6
b
Fig. 20. Two examples of variety 6-6, type (ii) neurons with axon projections to lamina 4Ca.Part (a)is from the outer operculum of area 17, in the
perimacular representation, whereas 05) is from the calcarine roof peripheral field representation. (See Fig. 18 and 19a for other examples.) Golgi
Rapid impregnationsfrom 3-week-old Macaca nernestrina. Scale bar = 100
pm.
LOCAL CIRCUIT NEURONS OF MONKEY VISUAL CORTEX
the 5A-5B region or between the 2-3A and 3B-4A regions
have not yet been clearly defined, but one would certainly
expect differences in function, given the very different circuitry that each region engages in.
For those 5B local circuit neurons whose bilaminar axon
distribution to 5B and 2-3A matches that of the 5B pyramidal neuron basal and apical dendritic fields, it might be
suggested that the correlation indicates a relationship; for
instance, the local circuit neurons may contribute input to
the two parts of the dendrite field of the 5B pyramidal
neurons. However, the relative lateral spreads of the local
axon arbors within 5B and in 2-3A can be quite different
for single axons; sometimes the 5B arbor is narrowly confined and the superficial arbor wide and sometimes it is the
reverse, with laterally wide spreading arbor in 5B and
narrow field in 2-3A. The branching pattern of the 5B axon
field can also be quite differently structured from the lamina 3A-2 field of the same axon. For instance, variety 5B-1
has an axon field within 5B that resembles that typical of
“basket” neurons; such axons have been described as contacting primarily cell bodies and dendritic initial segments;
in the case of these 5B-1neurons the spreading axon would
presumably make rather limited contact to each of rather
widely separated postsynaptic neurons. The superficial axon
arbor of the same axon is, however, confined to a quite
narrow but dense, cone-shaped arbor that seems spatially
suited to contact processes in a tight cluster, perhaps apical
dendritic terminal arbors. Since the descending axon trunks
of single layer 2-3A pyramidal neurons can give off collaterals that spread quite widely in 5B, another suggestion
might be that the 5B-1 local circuit neurons are reciprocally
related to tight clusters of 2-3A pyramidal neurons and to
the widely spread axon target sites in 5B of these same 23A neurons.
So far we have not traced any clear-cut axon projections
from 5B local circuit neurons to divisions of 4C or to 4B.
The investigation of interlaminar connections using small
HRP injections (Blasdel et al., ’85)showed a clear projection
from 4B to 5, which did not appear to be strongly reciprocated. Injections into 5B produced a coarse fiber population
rising into and spreading laterally within 4Ca and a more
narrowly focused light terminal labeling in 4B; for the
moment we are unable to explain these HRP-labeled projections to divisions of 4 on the basis of our Golgi-impregnated
neuron projections. However, if any of the local circuit neurons we have described within 5B were to be suspected of
projections to 4Ca, particularly its upper region, it might
be the 5B-5 variety whose coarse rising trunks have never
been traced to their superficial terminal zone (but seem to
lie higher than mid 4Ca since rising axon trunks have been
traced at least this far without branches) and whose local
axon arbor, and often the dendritic field, extend down
through layer 6, perhaps therefore justifying an arbor in
divisions of lamina 4.
Several varieties of the 5B local circuit neurons regularly
have axon trunks that descend and enter the white matter,
perhaps providing efferent projections from V1. In our earlier study of the local circuit neurons of laminae 5A and
4C, no axon trunks had been found to pass from these
neurons into the white matter; this had not surprised us for
even the excitatory spine-bearing neurons of these layers
do not appear to project out of the region. The relative
frequency of apparent efferent projections from the local
circuit neurons of lamina 5B does surprise us, although
efferent projections from local circuit neurons have been
25
reported previously, even by us (Lund et al., ’79). Since
lamina 5B contains pyramidal neurons projecting to mainly
subcortical destinations (e.g., superior colliculus, pulvinar,
and pons), it is possible that these same projections are
made by both local circuit (perhaps inhibitory) neurons 8s
well as pyramidal neurons (presumed t o be excitatory).
Double labeling studies with retrograde markers and GAD
or GABA antibodies could be used to investigate this question. We have not detected obvious efferent axon trunks
from the local circuit neurons of lamina 6, though perhaps
their profuse axon fields with axon collaterals that routinely reach into the adjacent white matter may have disguised such a contribution. Interestingly, we are finding
that local circuit neurons of the superficial layers, in at
least the 3A-2 region, also contribute axons to the white
matter.
Local circuit neurons of lamina 6
The local circuit neuron varieties we have seen in lamina
6 (see Fig. 22) have some differences in class compared to
those seen in layer 5B. For instance, we have regularly
found chandelier neurons in 5B but not in lamina 6, and
we have found pericellular “basket” neurons in 6 but not
in 5B. We do not know if this finding is real or if it is due to
the vagaries of sampling and staining of Golgi material,
but it is certainly worth watching out for examples of these
neurons in future studies of the deeper layers. Marin-Padilla (‘87) also failed to find chandelier cells in layer 6 of
human striate cortex, although they were present in layer
5 and in 4Ca upward, as we have also found in the monkey.
In the cat, however, at least the characteristic axon arbors
are seen in lamina 6, although sometimes they arise as
interlaminar projections from neurons in the Superficial
layers (Lund et al., ’79; Fairen and Valverde, ’80). It is also
worth noticing the similarity in dendritic form of the chandelier and pericellular basket neuron, despite the marked
difference in axon morphology. The forked distal dendritic
tips of both these varieties of neuron may conceivably be a
device for increasing dendritic surface area distally, which
might in turn allow a greater number of synapses distally,
thereby increasing the efficiency of inputs placed farther
from the soma and spike generating site.
For the local circuit neurons in lamina 6, there is much
more evident intrusion of dendritic and axonal processes
into lamina 5B than is seen to occur in the other direction,
from neurons of 5B into lamina 6. However, only those
neurons whose axons project above lamina 5 (variety 6-61
have dendrites crossing the 5-4 boundary. The axon projections of this variety of neurons distribute in the thalamic
recipient regions of 4C and 4A as well as to 5A and lower
3B, and therefore mimic those of the 5A-2 group of local
circuit neurons. We have elsewhere (Lund, ’88) pointed out
that the local circuit neurons of laminae 6, 5A, divisions of
4C and 4A all closely interrelate with each other in their
patterns of axon and dendritic distribution. Since the pyramidal neurons of lamina 6 also have apical dendritic processes and recurrent axon relays to these same more
superficial laminae (Lund and Boothe, ’75; Lund et al., ’77)
and the spiny stellate neurons of 4C have axon collaterals
that innervate 3Bl4A, 5A, and 6, it is reasonable to suspect
that these layers are in constant and close intercommunication in both excitatory and inhibitory fashion. One possible omission from the local circuit neuron axon projections
to 4C is a projection from layer 6 neurons to the lower half
of 4C& We may simply have missed impregnating such
1-81;
4Ca
3B
1
6-6 i
6 -1
6-4
6-5
6-3
a t least some of these laminar patterns of pyramidal neuron dendritic and
axon distribution. Varieties of local circuit neurons in lamina 5A also mimic
these projections (see variety 5-2 in Lund, '87; and Fig. 4a in this study).
6-2
Fig. 22 Summary diagram of local circuit neuron varieties described for
lamina 6. Pyramidal neurons of lamina 6 show recurrent axon projections
and apical dendritic arborizations in divisions of 4C, in 4A/3B, and in 5A.
The 6-6 (i-ii) local circuit neuron axon projections can be seen to replicate
6-6ii
v
28
cells but so far none have been identified that provide a
clear and dense projection to this region.
Interrelations between layers 5A and 5B may be present
for 5B neurons merely in terms of the small degree of
overlap into 5A made by the processes of many 5B local
circuit neurons. However, for some varieties of 5A neuron
this interrelation may be more carefully structured. For
instance, the spread of 5A-3 (Lund, '87) chandelier neuron
dendrites through the depth of 5B suggests these neurons
are accepting synaptic input within 5B even though their
axon distribution favors lamina 5A. In addition, the 5A-2
neurons described here and in our earlier report (Lund, '87)
can have a reasonable portion of their descending dendrites
passing through layer 5B before entering layer 6 with the
possibility that they may accept some input from the 5B
region.
The special orientation of one variety of neurons (5B:6-1)
along the junctional border of laminae 5B and 6 suggests
this region to have a special function. We know that the
majority of the neurons projecting to cortical area MT, including the largest pyramidal neurons of the striate cortex
(which have been shown by Fries et al. ('85) to send collaterals axon projections to both MT and the colliculus) have
somata in upper lamina 6 and on the border with lamina
5B. The pericellular basket axons have the majority of their
contacts on large pyramidal neurons in this same upper
6-5B border region. It is also known that the property of
direction selectivity is especially emphasized in cortical
area MT and therefore perhaps a quality shown by at least
the largest pyramidal neurons whose somata lie at the
border region if not other smaller cells in the same region.
Since, in the monkey, neurons of layer 6, rather than those
of layer 5, have been found to show direction selective
properties (Hubel and Wiesel, '68; Dow, '74; Livingstone
and Hubel, '84; Orban et al., '86; Hawken et al., '88), there
is some uncertainty in our minds over the relationship of
local circuit neuron varieties and the property of direction
selectivity. If inhibitory circuits are involved, the border
5B:6-1 basket neurons may be good candidates and the
pericellular basket neurons (6-2)are strategically placed for
such activity. However, other basket cells of layer 6 also
emphasize axon contributions to the upper portion of 6 and
it is impossible to say at the moment which of these circuits
may contribute to this important property. We earlier (Lund,
'87) pointed out that laminae 4C has "basket" neurons (-6
variety) that contribute laterally wide spreading arbors in
upper 4C, 4B, and 4A; this region is the only zone, other
than lamina 6, of monkey striate cortex showing direction
selective properties. These local circuit basket neurons of
4C are the only candidate so far described for long lateral
inhibitory connections in this upper zone and they somewhat resemble the 5B:6-1 variety except their dendrites are
less laterally extended.
It should be remembered that throughout this study we
have been describing immature neurons. Further maturational changes will certainly occur in both axons and dendrites. For the axons, the number and size of terminal
boutons and their synaptic contacts are known to change
with age (Lund et al., '77; Mates and Lund, '83). The size of
the intralaminar terminal arbors may also change. However, we suspect that the pattern of interlaminar projections and the choice of postsynaptic target is established
early in development and then remains consistent into
adulthood. The dendritic arbors may alter in the richness
of their branching or total length and the spicules and
J.S. LUND ET AL.
spines that are a common feature of these immature interneurons are greatly reduced in number or entirely lost
during maturation (Morest, '69; Marin-Padilla, '72; Lund
et al., '77). Further study is needed, however, to determine
what precise maturational changes may occur for specific
neuron types.
ACKNOWLEDGMENTS
This work was supported by National Eye Institute grant
EY05282 and NATO grant 0167185. We thank Tom Harper
and Suzanne Holbach for excellent technical assistance,
and Roberta Erickson for preparation of the manuscript.
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