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The Journal of Neuroscience, October 1, 1998, 18(19):8086-8094
Ascending Projections of Simple and Complex Cells in Layer 6 of
the Cat Striate Cortex
Judith A.
Hirsch,
Christine A.
Gallagher,
José-Manuel
Alonso, and
Luis M.
Martinez
Laboratory of Neurobiology, The Rockefeller University, New York,
New York 10021
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ABSTRACT |
Receptive field properties vary systematically across the different
layers of the cat striate cortex. Understanding how these functional
differences emerge requires a precise description of the interlaminar
connections and the quality of information that they transmit. This
study examines the contribution of the two physiological types of
neuron in layer 6, simple and complex, to the cortical microcircuit.
The approach was to make whole-cell recordings with dye-filled
electrodes in vivo to correlate visual response property
with intracortical projection pattern. The two simple cells we stained
projected to layer 4, as previously reported (Gilbert and Wiesel, 1979 ;
Martin and Whitteridge, 1984). Six of the eight complex cells that we
labeled projected to the superficial layers, a pathway not previously
described in the cat. The remaining two cells targeted the
infragranular layers. Layer 4 is dominated by simple cells, whereas
layers 5 and 2+3 are mainly composed of complex cells (Hubel and
Wiesel, 1962; Gilbert, 1977). Hence, our results indicate that the
ascending projections of simple cells in layer 6 target other simple
cells. In parallel, the ascending projections of a population of
complex cells in layer 6 favor other complex cells. Anatomical
experiments in several species (Lund and Boothe, 1975; Burkhalter,
1989; Usrey and Fitzpatrick, 1996; Wiser and Callaway, 1996) had also
demonstrated that layer 6 gives rise to two separate intracortical
pathways. Pooling the results of these anatomical studies with our own
suggests a common feature of the laminar organization: cells that
project to different intracortical targets have distinct functional
characteristics.
Key words:
visual cortex; patch recording in vivo; simple
cell; complex cell; layer 6; pyramidal cell
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INTRODUCTION |
We are interested in how visual
information is coded by the different elements of the cortical
microcircuit. With the striking exception of layer 6, each layer in the
cat striate cortex is mainly composed of one physiological cell type,
simple or complex (Hubel and Wiesel, 1962; Gilbert, 1977; Gilbert and
Wiesel, 1981; Grieve and Sillito, 1995; see Fig. 6). Simple cells
dominate layer 4, the principal target of the lateral geniculate
nucleus; their receptive fields are built of adjacent subregions
arranged so that neighbors prefer stimuli of the opposite contrast
(Hubel and Wiesel, 1962; Gilbert, 1977). The laminae that receive
little input from the thalamus, layer 2+3, and layer 5, are largely
composed of complex cells, neurons whose receptive fields lack
spatially separate subregions (Hubel and Wiesel, 1962; Gilbert, 1977).
Layer 6 is divided into two tiers, as distinguished by the pattern of thalamic innervation (LeVay and Gilbert, 1976). The upper stratum receives appreciable contact from the geniculate and contains a mix of
simple and complex cells. The lower aspect derives its chief input from
intracortical sources and is populated by complex cells (Hubel and
Wiesel, 1962; Gilbert, 1977; Grieve and Sillito, 1995).
In keeping with their physiological uniformity, layers 2+3, 4, and 5 each have one principal laminar target. Layer 4 projects to 2+3, which
directs its output to layer 5; layer 5, in turn, projects to layer 6 (Gilbert and Kelly, 1975; Gilbert and Wiesel, 1979; Lin et al., 1979;
Martin and Whitteridge, 1984; McGuire et al., 1984). Based on the
projection patterns of just a handful of labeled cells in layer 6 in vivo, it was thought that the entire interlaminar output
was directed to layer 4. We have characterized the receptive field
structure and projection pattern of simple and complex cells throughout
the depth of layer 6. The approach was to combine whole-cell recording
with intracellular staining in vivo. The simple cells we
labeled targeted layer 4, as previously reported (Gilbert and Wiesel,
1979; Martin and Whitteridge, 1984). By contrast, the complex cells we
stained had a different projection pattern. These directed the bulk of
their output to the laminae composed of complex cells, layers 5 and
2+3, rather than to layer 4. Thus, a population of complex cells in
layer 6 provides an ascending projection to the superficial layers
distinct from the path that leads from layer 6 to layer 4.
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MATERIALS AND METHODS |
Anesthesia. Nine adult cats, 2.5-3.5 kg, were
anesthetized with ketamine (10 mg/kg, i.m.) followed by thiopental
sodium (20 mg/kg, i.v.), supplemented as needed. Lidocaine was applied
topically at all incisions or points of pressure. Temperature
(37°-38°C), EKG, EEG, and expired CO2 (27-33 mmHg)
were monitored throughout the experiment. Anesthesia was maintained by
continuous infusion of thiopental sodium (2-4 mg · kg · hr,
i.v.) adjusted as indicated by the EEG and EKG. After the completion of
surgery, animals were paralyzed [vecuronium bromide (Norcuron) 0.2 mg · kg · hr, i.v.] and respired artificially.
Surgery. An endotracheal tube was introduced through a
tracheotomy before the animal was placed in a stereotaxic apparatus. Then, a cortical craniotomy centered on Horsley-Clark coordinates P3-L2 was made to expose the longitudinal gyrus. After dilating the
pupils (1% atropine sulfate) and retracting the nictitating membranes
(10% phenylephrine), the eyes were refracted and fitted with contact
lenses to focus on a tangent screen. The position of the area centralis
and the optic disk of each eye was determined with a fundus camera.
Before recording, the dura was reflected, and the cortex was covered
with agarose.
Acquisition of visually evoked responses. Intracellular and
extracellular records were collected by a computer running the Discovery software package (Datawave Systems, Longmont, CO);
intracellular records were normally sampled at 3-4 kHz. An
AT-vista board (Truevision, Indianapolis, IN), controlled by the
same computer that received the data, generated visual stimuli that
were presented on a computer monitor (frame rate, 100, 105, 128, or 140 Hz). Each cycle of the stimulus protocol consisted of light or dark
squares at various contrasts (range, 30-70%) flashed singly for
29-39 msec in pseudorandom order, 16 times on a 16 × 16 grid
(sparse noise; Jones and Palmer, 1987). Grid spacing ranged from 0.4 to
0.85° and square size from 0.4 to 1.7°.
Determination of receptive fields. Depolarizations evoked by
bright stimuli were termed "on" responses and those to
dark stimuli, "off" responses. Receptive fields
with separate and adjacent on and off subregions
were classified as simple; those that lacked segregated on
and off responses were considered complex (Hubel and Wiesel,
1962; for review, see Skottun et al., 1991). To generate maps of the
simple receptive fields, responses to dark stimuli were subtracted from
bright ones. For complex cells, separate maps of bright and dark
responses were made. All fields shown were smoothed by one half
pixel.
Recording. Patch-pipette resistance was  12 M when
filled with internal solution, in mM: K gluconate, 120;
NaCl, 5; CaCl2, 1; MgCl2, 1;
EGTA, 11; GTP, 0.2; ATP, 2; HEPES, 40; and biocytin 1%, pH 7.3, 290 mOsm (Malinow and Tsien, 1990). Initial seal resistances were 0.5-1.0
G. Recordings were made with an Axopatch 200A amplifier (Axon
Instruments, Foster City, CA) and stored as described above; neither
capacitance nor access resistance was compensated, so fast spikes were
filtered. Because the access resistance often increased after rupture
of the membrane (Edwards and Konnerth, 1992), the voltages recorded
were sometimes divided (Stühmer et al., 1983).
Histology. After histological processing (Horikawa and
Armstrong, 1988; Hirsch, 1995), labeled neurons were drawn using a camera lucida, or a computerized three-dimensional reconstruction system, (MicroBrightfield, Colchester, VT).
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RESULTS |
Physiological differences between simple and complex cells in
layer 6
The response patterns of simple cells and complex cells are
illustrated in Figure 1. Simple receptive
fields comprise adjacent on and off subregions;
within each subregion stimuli of reverse contrast evoke responses of
the opposite sign (Hubel and Wiesel, 1962; Jones and Palmer, 1987;
Ferster, 1988, Hirsch et al., 1995). Postsynaptic responses to stimuli
flashed within the on subregion of a layer 6 simple cell are
shown in Figure 1A; the receptive field map above the
traces indicates stimulus position. Each presentation of a bright
square evoked a strong depolarization; a slight hyperpolarization and
excitatory rebound followed the withdrawal of the stimulus. Dark
squares elicited a hyperpolarization followed by an excitatory rebound.
Responses from the off subregion were similar except that
dark stimuli were excitatory, and the bright ones were inhibitory (data
not shown). This "push-pull" pattern of response is also common to
simple cells in layer 4 and its borders (Hirsch et al., 1995).
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Figure 1.
Synaptic responses of simple and complex cells in
layer 6. The receptive field of a layer 6 simple cell had a small
off subregion left of a stronger on subregion
(A, top). The dotted
square indicates the peak of the on subregion. The
left and right panels beneath the map each show three individual trials
of a bright or dark stimulus that fell over the peak of the
on subregion; the averaged response of all sixteen trials of
each stimulus is shown in bold. The thick
bar under every trace marks stimulus duration. The essential
features of the response pattern are that the bright stimuli initiated
a strong depolarization (A, bottom left),
whereas dark stimuli flashed at the same spot elicited
hyperpolarizations (A, bottom right).
B illustrates responses of a typical complex cell in
layer 6. Its receptive field (B, top) was
constructed from responses to dark stimuli because bright squares had
limited action. The responses evoked by dark squares falling in the
peak of the field (dotted square) were small, brief
depolarizations (B, bottom right). There
was no response to the introduction of bright squares, although a weak
depolarization occasionally followed stimulus withdrawal
(B, bottom left).
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Although complex receptive fields are far more varied than those of
simple cells (Hubel and Wiesel, 1962; Gilbert, 1977; Movshon et al.,
1978; Palmer and Davis, 1981; Ohzawa and Freeman, 1986), they share a
common characteristic: their receptive fields are not divided into
subregions. The map at the top of Figure 1B shows the
field of a complex cell that responded to dark stimuli; these evoked a
brief depolarization (Fig. 1B, bottom
right). Bright spots were essentially ineffective, with only
a faint response to withdrawal of the stimulus (Fig.
1B, bottom left). This sort of
response pattern was the most common in our sample (see Figs. 3A,B, 5B). Variations
among cells included responses dominated by inhibition rather than
excitation (see Fig. 4A), insensitivity to the
flashed stimuli (see Figs. 4B, 5A; fields
were mapped with moving bars) or overlapping on and
off responses (data not shown). As yet, we have not detected
physiological trends that correlate with the different projection
patterns of the complex cells that we describe below.
Projections of simple cells
We found that simple cells in layer 6 had dendrites and axons that
arborized densely in layer 4, as previously described (Gilbert and
Wiesel, 1979; Martin and Whitteridge, 1984). Maps of the receptive fields are shown above the reconstructions. The cell pictured in Figure
2A was located in
middle of layer 6. Its basal dendritic arbor spread densely within
~100 µm of the soma; the apical dendrite fanned into long branches
that traversed the depth of layer 4. Axonal projections were sparse
near layer 6; they became more elaborate as they entered layer 4 to
innervate its upper half. A second simple cell sat at the border
between layers 5 and 6 (Fig. 2B). Its basal dendrites
were rooted in layer 6; its apical dendrite and its apical arbor split
into a few vertical branches in layer 4. Unlike the neuron in Figure
2A, this cell directed horizontal connections in
layer 6. In sum, for simple cells, the dendrites and axons tended to
ramify in the vicinity of other simple cells, that is, in regions where
the afferents from the dorsal layers (A, A1) of the lateral geniculate
terminate (see Fig. 6).
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Figure 2.
Projections of simple cells in layer 6. The
receptive fields of two simple cells are shown above the anatomical
reconstructions. The receptive field in panel A is the same as in
Figure 1A. The cell was located in the middle of
layer 6 and projected densely to layer 4. A second cell had a receptive
field comprising a strong off subregion flanked by a weaker
on subregion. This cell also projected to layer 4; in
addition, it made horizontal connections within layer 6 itself. Both
neurons had descending collaterals that appeared to leave area 17. Grid
spacing was 0.4° for A and 0.85° for
B.
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Projections of complex cells
For the complex cells we labeled, the projection pattern was
distinctly different from that for simple cells and demonstrates a
novel component of the cortical microcircuit. Instead of ending in
layer 4, the complex cells directed the majority of their output to
layer 2+3 or layer 5. That is, they targeted regions that are populated
by other complex cells and that receive input from the ventral (C)
layers of the geniculate and extrageniculate nuclei (see Fig. 6). The
projection patterns we have observed so far cluster into three groups:
cells that favor the lower aspect of layer 2+3, those preferring the
upper tier of layer 2+3, and those that send stronger projections to
the infragranular (layers 5 and 6) than to the supragranular (layer
2+3) layers.
Cells favoring the lower aspect of layers 2+3
Two complex cells that directed their output to the lower tier of
layer 2+3 are drawn in Figure 3. The soma
of one cell lay at base of the layer (Fig. 3A); its basal
dendrites spread near the soma, with a few reaching into the white
matter. The apical dendrite approached layer 1 but did not branch after
leaving layer 5. Axonal arbors remained fairly sparse until reaching
the border between layers 4 and 2+3. There they divided frequently,
with most shoots innervating lower layer 2+3. A second cell with a similar projection pattern is pictured in Figure 3B. Its
soma also occupied the lower part of the layer. With the exception of a
shorter apical process, the dendritic arbor was much like that seen in
Figure 3A; it avoided regions supplied by the primary afferents. The axon gave off short collaterals in layers 6 and 5 before
traveling through layer 4. As for the cell in Figure 3A,
axonal branching was densest at the upper border of layer 4 and lower
layer 2+3. A collateral that left the home column formed a separate
cluster in the superficial layers. Last, the axons of both of these
cells seemed to end in the white matter rather than exiting area
17.
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Figure 3.
Complex cells in layer 6 that direct their densest
output to the lower aspect of the superficial layers. Both cells were
located in lower layer 6 and sent much of their output to the border
between layers 4 and 2+3, and lower layer 2+3. The cell drawn in
B gave off prominent collaterals that traveled outside
the home column to synapse in the superficial layers. Neither cell
seemed to project beyond the white matter. Grid spacing was 0.85°;
both maps were constructed from responses to dark stimuli because those
alone were effective. Intracellular records from the cell pictured in
B are seen in Figure 1B.
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Cells favoring the upper aspect of layer 2+3
Figure 4A shows a
striking example of a cell that favored the upper tier of the
superficial layers; its soma was near the top of layer 6. The basal
dendrites formed a radial array that extended well into layer 5, and
the apical dendrite ended in a compact tuft in layer 1. A dense axonal
plexus wove around the basal dendrites, with several collaterals
ascending to layer 2+3 (one ascending trunk rose only so far as layer
4). Once in the upper half of the superficial layers, these axons split
into many short processes that ended within ~100 µm of the apical
dendrite. The cell also directed a prominent collateral outside of the
home column, as in Figure 3B. A second cell, located in the
middle of the layer, sent local dendrites throughout the laminar depth and into the white matter; its apical dendrite reached the middle of
layer 2+3. Ascending axons loosely spiraled the apical dendrite, sending numerous twigs in layers 6 and 5 and few in lower layer 4. The
main collaterals continued on a path to the superficial aspect of layer
2+3 where they forked into long branches that reached the pia. Two
additional cells (data not shown) were located at the bottom of layer 6 and had dendrites that reached layer 1. One sent a sparse projection
that reached layer 1; the axon of the other terminated in a thick spray
within the upper aspect of layer 2+3. Three of the four cells had axons
that appeared to exit area 17.
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Figure 4.
Complex cells in layer 6 whose projections target
the upper tier of the superficial layers. The cell drawn in
A projected densely to the top half of the superficial
layers. The projection included a dense axonal arborization in vertical
register with the apical dendrite and a prominent secondary cluster
that lay outside the home column. The receptive field map shows
responses to dark stimuli; it has an inverse shading pattern to
indicate that the net response was inhibitory rather than excitatory
(responses to bright stimuli were weak and are not shown); grid spacing
was 0.85°. The cell drawn in B also had axon
collaterals that reached the pia. This neuron failed to respond to the
flashed squares and was mapped by hand with moving light bars. Each of
these cells appeared to leave area 17.
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Cells favoring infragranular layers
The remaining two complex cells were somewhat different from those
previously shown. The cell drawn in Figure
5A was located near the bottom
of layer 6. It gave off small basal and apical dendritic branches in
layers 6 and 5, then the apical dendrite took a straight course to
layer 2+3, where it bifurcated, with each limb nearing the pia. The
axon ramified thickly through layers 5 and 6 while a rare process
entered layer 4. Only one collateral traversed the depth of the
granular layer to end at the upper border. An unusual pyramidal cell
was located in lower layer 6, Figure 5B. Its basal dendrites
(some too pale to trace) were directed horizontally, and its apical
dendrite reached layer 5. The axons rambled for nearly a millimeter at
each side of the soma. The majority of the collaterals took a
horizontal course after leaving one of the principal trunks. The many
short branches that fringed the main processes indicated a high degree
of connectivity throughout the arbor. The thickest bundle of fibers ran
along the top of layer 5; a substantial meshwork spread though layer 6 as well. Additional projections included a central spray of terminals
shot from layer 4 to layer 2+3 and sparser collaterals in the middle of
layer 4 and its upper border. Neither of the cells drawn in Figure 5
seemed to have axons that exited area 17.
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Figure 5.
Layer 6 complex cells that terminate most heavily
in the infragranular layers. Although these two cells were different in
many regards, they shared a preference for layers 5 and 6. Neither
seemed to project beyond area 17. The cell seen in A did
not respond to flashed stimuli and was mapped by hand with moving light
bars. The map in B was constructed from off responses
because bright stimuli were not effective; grid spacing was
0.85°.
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DISCUSSION |
Layer 6 of the cat visual cortex includes two physiological
classes of neuron, simple and complex. Simple cells are restricted to
the upper tier of the layer, whereas complex cells populate its full
thickness (Gilbert, 1977). It had previously been thought that layer 4 was the common target of all the pyramidal cells in the layer 6 (Gilbert and Wiesel, 1979; Martin and Whitteridge, 1984; McGuire et
al., 1984). We have found a novel projection from layer 6 by which some
complex cells direct their output to the superficial layers. Hence, the
functional diversity of layer 6 is reflected in distinct interlaminar
patterns of connectivity.
Intracortical connectivity
Intracolumnar connections
Our principal finding is that complex cells in layer 6 send much
of their output to regions populated by other complex cells, that is,
to layers 2+3 and 5. Moreover, this complex cell pathway is distinct
from the one made by simple cells, which supplies dense input to layer
4 (Gilbert and Wiesel, 1979; Martin and Whitteridge, 1984; Fig. 2 this
study). Six of the eight complex cells studied projected to the
superficial layers. Of these, four preferred the upper aspect of layer
2+3, and two preferred the lower tier. The remaining cells shared a
preference for the infragranular layers. It seems reasonable to
conclude that the superficial layers receive strong input from layer 6, although our sample remains too small to permit an exact estimation of
the relative weight of ascending input that each layer or sublamina
receives.
It is important to mention that not every complex cell in layer 6 favors layers containing other complex cells. McGuire et al. (1984)
illustrate two complex cells whose projection patterns resemble those
made by simple cells. Complex cells fall into two groups, based on
their station in the cortical microcircuit: first order cells receive
substantial direct input from the thalamus and second order cells do
not (Hoffman and Stone, 1971; Bullier and Henry, 1979; Ferster and
Lindström, 1983). In a study of the superficial layers, we
recently reported that first and second order complex cells have
distinct synaptic physiologies (Hirsch et al., 1997). That is, the
visual responses of first order complex cells, like those of simple
cells, reliably capture the pattern of thalamic input. By contrast, the
behavior of second order cells is variable and unpredictable. The
response patterns of the layer 6 complex cells included in the current
study resemble the records made from second order cells. Perhaps
McGuire et al. (1984) recorded from a different physiological
population of layer 6 complex cells, one that receives substantial
direct input from the thalamus. In keeping with this idea, the complex
cells illustrated in McGuire et al. (1984), like all layer 6 simple
cells labeled in vivo (Gilbert and Wiesel, 1979; Martin et
al., 1984; Fig. 2), had basal and apical dendritic branches that
ramified within upper layer 6 and layer 4, where the fibers from the
dorsal layers of the lateral geniculate terminate. The complex cells
that we labeled branched less frequently in these regions.
Extracolumnar projections
In addition to their role in local processing, projections from
layer 6 appear to convey information across visual space. Four of the
complex cells we filled sent collaterals outside of their own column to
form superficial clusters in adjacent zones. These clusters were
comparable in size and spacing to those made by the horizontal
connections that course within layers 5 and 2+3 (Gilbert and Wiesel,
1979, 1983; Martin and Whitteridge, 1984; Gilbert and Wiesel, 1989);
albeit the intralaminar collaterals span larger distances (Gilbert and
Wiesel, 1983).
Simple cells in layer 6 are also known to direct collaterals that
terminate in layer 4, at a distance from the home column (Martin and
Whitteridge, 1984; Katz, 1987). We have found evidence of another
extracolumnar path, a simple cell that sent lateral connections to
layer 6 itself (Katz, 1987). This finding complements the previous
observation of a layer 4 simple cell that sent horizontal collaterals
in layer 6 (Hirsch et al., 1995). Hence, there appears to be an
interlaminar feedback circuit by which simple cells integrate information across cortical columns. This circuit may help to build the
long, simple receptive fields occasionally encountered in layer 4 (Jagadeesh and Ferster, 1990) and layer 6 (Gilbert, 1977; Grieve and
Sillito, 1991, 1995).
Lamination in cat cortex
In the primate and tree shrew, fine-grained laminar subdivisions
are obvious even from the distribution of cell bodies. This is not the
case for the cat. The sublaminar preferences in axonal projection seen
in this study, together with illustrations provided by others (Gilbert
and Wiesel, 1979, 1983; Lin et al., 1979; Martin and Whitteridge,
1984), indicate that the cat has a higher degree of laminar
organization than is evident from the cytoarchitecture alone. As yet,
however, it is not clear that the position of a given cell in the depth
of layer 6 predicts the sublaminar preference of its output.
Subcortical connectivity
Claustral targets
Cells in layer 6 are known to project to the visual claustrum
(LeVay and Sherk, 1981; Katz, 1987); many of these have long apical
dendrites that reach layer 1. Physiological studies show that
corticoclaustal cells have simple receptive fields (Grieve and Sillito,
1995). Given that the only cells we labeled that had long dendrites
were complex, it is unlikely that we recorded from claustral projecting
cells, which make up 3-5% of the layer 6 population.
Thalamic targets
In cat, ~50% of the cells in layer 6 project to the geniculate;
these are scattered through the full depth of the layer (Gilbert and
Kelly, 1975; McCourt et al., 1986; Katz, 1987), and most of these have
simple receptive fields (Grieve and Sillito, 1995). Katz (1987)
characterized two types of geniculate projecting cells in
vitro. The most common type had dendrites that extended long branches in layer 4 and resembled the simple cells that we and others
have filled (Gilbert and Wiesel, 1979; Martin and Whitteridge, 1984;
Fig. 2). The other class of corticothalamic cell had sparse apical
dendrites that rose no further than layer 3 (presumably the superficial
axonal arbors were severed when the slices were cut); these recall one
of the complex cells we stained (Fig. 4B). Thus, it
appears that our sample included both simple and complex geniculocortical cells.
Comparative anatomy
Results of anatomical studies in other species give the sense that
parallel ascending and descending projections from layer 6 are
phylogenetically preserved features of the mammalian visual pathway.
Moreover, there is a certain reciprocity in the flow of information
between the cortex and thalamus. In one circuit, cells in upper layer 6 direct some axonal collaterals up to layer 4 and others down to the
dorsal layers of the geniculate: there, relay cells project back to the
upper subtier of layer 6 and to layer 4 (rat, Burkhalter, 1989;
galago, Conley and Raczkowski, 1990; macaque, Lund et al., 1975, 1979;
Fitzpatrick et al., 1985, 1994; Wiser and Callaway, 1996). A second
group of cells, at the base of layer 6 (rat, Burkhalter, 1989;
Boursassa and Deschenes, 1995; galago, Conley and Raczkowski, 1990) or
distributed throughout its depth (macaque, Fitzpatrick et al., 1985;
Wiser and Callaway, 1996) provides ascending input to the supragranular
layers and descending axons to the ventral and koniocellular layers of
the geniculate and extrageniculate nuclei (for review, see Lund, 1988; Casagrande, 1994; Fitzpatrick, 1996; Callaway, 1998). These thalamic divisions project back to the supragranular layers in turn (rat, Bourassa and Deschenes, 1995; galago, Conley and Raczkowski, 1990; macaque, Fitzpatrick et al., 1994). The divergence in the input and
output of layer 6 is best appreciated in the tree shrew. There, upper
layer 6 targets the granular layers and the specific subset of
geniculate laminae that supply them. A correspondent feedback circuit
links lower layer 6 with the supragranular layers and with the
remaining geniculate laminae and pulvinar (Usrey and Fitzpatrick,
1996).
Information flow in the projections to and from layer 6 in cat
Taking the earlier studies (Lund and Boothe, 1975; Lund et al.,
1975; Gilbert and Wiesel, 1979; McGuire et al., 1984; Martin and
Whitteridge, 1984; Fitzpatrick et al., 1985, 1994; Burkhalter, 1989;
Conley and Raczkowski, 1990; Casagrande, 1994; Bourassa and Deschennes,
1995; Sawatari and Callaway, 1996; Usrey and Fitzpatrick, 1996; Wiser
and Callaway, 1996) together with our own suggests a pattern of
ascending and descending projections from layer 6 that is outlined in a
summary diagram (Fig. 6). The projections are divided into two, loosely parallel feedback circuits. One involves
the layer 6 complex cells that project to laminae 5 and 2+3 (Fig. 6,
filled arrows). These cells receive input from the ventral layers of the lateral geniculate and the extrageniculate nuclei; subcortical information arrives directly via the apical dendrites or is relayed by overlying complex cells (LeVay and Gilbert,
1976; Miller et al., 1980; Bullier et al., 1984). The path is closed by
the descending projections from the layer 6 complex cells to the same
thalamic sources. A second loop (open arrows)
interconnects the dorsal layers of the geniculate and their principal
cortical targets (simple cells and, perhaps, a subgroup of complex
cells) (Gilbert and Wiesel, 1979; Robson, 1983; Boyapati and Henry,
1984; McGuire et al., 1984; Humphrey et al., 1985; Ferster, 1990; Ahmed
et al., 1994; Grieve and Sillito, 1995; Murphy and Sillito, 1996). The
two pathways overlap to an extent; one clear example is that the
complex cells that project to the superficial layers provide some input
to layer 4. A larger sample of layer 6 cells is required to understand
exactly the pattern of information that these two circuits
exchange.
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Figure 6.
Thalamocortical feedback circuits involving the
simple or the complex cells of layer 6. The extent and weight of the
simple (white) and complex (black) cell
populations in each cortical layer are indicated by the length and
width of the pointed bars at the left of the diagram.
The major intracortical pathways are denoted by arrows
with solid shafts and presumed descending projections
are represented by arrows with dotted
shafts. Open arrowheads indicate projections by
simple cells, and filled arrows depict projections by
complex cells. Thalamorecipient cortical zones are
shaded. Dark gray codes regions contacted
by the A layers of the lateral geniculate nucleus, light
gray shows the projection from the C laminae, and
stippling denotes input from extrageniculate nuclei such
as the pulvinar and medial interlaminar nucleus.
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The effect of the projection from layer 6 complex cells to the
superficial layers remains to be explored. The axons that ascend from
layer 6 to layer 4 synapse selectively with dendritic shafts (McGuire
et al., 1984; Somogyi, 1989; Ahmed et al., 1994) and appear to contact
a higher proportion of smooth cells (McGuire et al., 1984; cf. Ahmed et
al., 1994) than do other cortical pathways; these, by and large, favor
dendritic spines (McGuire et al., 1991; Johnson and Burkhalter, 1996).
Hence, although the synapses made by the layer 6 pyramids are
themselves excitatory (Ferster and Lindström, 1985), they have
the potential to exert strong inhibitory influence in layer 4 via
smooth interneurons (McGuire et al., 1984; Bolz and Gilbert, 1986;
Hirsch, 1995). We hope to learn if the projection from layer 6 to the
superficial laminae shares the same target preferences as the
counterpart path to layer 4.
| |
FOOTNOTES |
Received May 28, 1998; revised July 21, 1998; accepted July 22, 1998.
This work was supported by National Institutes of Health Grants EY09593
(J.A.H.) and EY05253 (T.N.W.), the Klingenstein Fund (J.A.H.), and the
Human Frontiers Science Program Organization (L.M.M.). We are grateful
to Torsten N. Wiesel for support and advice during all phases of the
project. We thank R. Clay Reid for contributing the software to
generate the visual stimuli and to view the intracellular records.
Kathleen McGowan, Johanna L. Kornblum, and Komal A. Desai provided
superb technical support and helped to reconstruct some of the labeled
neurons. Peter Peirce photographed the drawings patiently and
precisely. We are indebted to W. Martin Usrey for advice in early
stages of the project and for his many thoughtful criticisms of this
manuscript.
Correspondence should be addressed to Judith A. Hirsch, Box 138, Laboratory of Neurobiology, The Rockefeller University, 1230 York
Avenue, New York, NY 10021.
| |
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Top
Abstract
Introduction
