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The Journal of Neuroscience, November 15, 1998, 18(22):9489-9499
Functional Streams and Local Connections of Layer 4C Neurons in
Primary Visual Cortex of the Macaque Monkey
N. Harumi
Yabuta and
Edward M.
Callaway
Systems Neurobiology Laboratories, The Salk Institute for
Biological Studies, La Jolla, California 92037
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ABSTRACT |
The primate visual system is composed of multiple, functionally
specialized cortical areas. The functional diversity among areas is
thought to reflect different contributions from early parallel visual
pathways to the area V1 neurons providing input to "higher"
cortical areas. The M pathway is believed to provide information about
motion and contrast, via layer 4B of V1, to dorsal visual areas. The P
pathway is believed to provide information about shape and color, via
layer 2/3 of V1, to ventral visual areas, with specialized
contributions from cytochrome-oxidase (CO) blob versus interblob
neurons. However, the detailed anatomical relationships between the M
and P pathways and the neurons in V1 that provide input to higher
extrastriate cortical areas are poorly understood. To study these
relationships, spiny stellate neurons in the M- and P-recipient layers
of V1, 4C and 4C , respectively, were intracellularly labeled, and
their axonal and dendritic arbors were reconstructed. We find that
neurons with dendrites in upper layer 4C project axons to layer 4B
and CO blobs in layer 2/3, thus relaying M input to these regions.
Other neurons in lower layer 4C provide M input to interblobs. These
cells have either (1) dendrites restricted to lower layer 4C and
axons specifically targeting layer 2/3 interblobs, or (2) dendrites in
lower 4C and 4C and axons targeting blobs and interblobs.
P-recipient layer 4C neurons have dense axonal arbors in both blobs
and interblobs but not layer 4B. Quantitative analyses reveal that
4C cells provide approximately five times more synapses than 4C
cells to layer 4B, whereas 4C cells provide five times more synapses than 4C cells to layer 2/3. These observations imply that M input is
dominant in layer 4B. In layer 2/3, both blobs and interblobs receive M
and P input, but the P input is dominant, and M input to interblobs
derives exclusively from a subpopulation of M afferents that targets
lower 4C, not from afferents targeting only upper 4C (cf. Blasdel
and Lund, 1983 ). We speculate that the M and P pathways to interblobs
are "X-like" linear systems, whereas blobs also receive nonlinear
"Y-like" M input.
Key words:
functional streams; local circuits; macaque; primary
visual cortex; primate; V1
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INTRODUCTION |
The relative contributions of the
functionally distinct M and P pathways are believed to be important
determinants of the functional differences between extrastriate
cortical areas (Livingstone and Hubel, 1988; for review, see Merigan
and Maunsell, 1993). Nevertheless, the actual relationships between the
M and P streams and V1 neurons projecting to extrastriate cortex are
poorly understood. We have addressed these relationships by studying
spiny stellate neurons in layer 4C of V1, because they lie at the heart
of the problem; they provide a direct link from LGN afferents to
extrastriate projection neurons.
In the retino-geniculo-cortical system, parallel M and P pathways
converge on V1, where they segregate their inputs into layers 4C and
4C, respectively (Hubel and Wiesel, 1972; Hendrickson et al., 1978;
Blasdel and Lund, 1983). Layer 4C neurons connect to neurons in more
superficial layers (layers 2-4B) (for review, see Callaway, 1998), and
these superficial neurons provide output, both directly and indirectly,
to functionally specialized extrastriate cortical areas (for review,
see Felleman and Van Essen, 1991). Specifically, neurons in layer 4B of
V1 provide direct and indirect input to dorsal visual areas believed to
be involved in computations about spatial relationships and motion in
visual scenes. Layer 2/3 can be subdivided into cytochrome-oxidase
(CO)-rich blob and interblob regions, which project in parallel to
ventral visual areas specialized for visual object identification (for
review, see Desimone and Ungerlieder, 1989; Felleman and Van Essen,
1991).
Based on differences in response properties, it has been suggested that
blobs might receive input from both the M and P pathways, whereas
interblobs are influenced primarily by the P pathway (Livingstone and
Hubel, 1988; Edwards et al., 1995). In particular, blob neurons have
better contrast sensitivity and are, on average, selective for lower
spatial frequencies than are interblob neurons (Tootell et al.,
1988a,b,c; Edwards et al., 1995), properties more like those of
magnocellular LGN neurons or M-recipient layer 4C cells than neurons
in the P pathway (Kaplan and Shapley, 1982; Blasdel and Fitzpatrick,
1984). These relationships received anatomical support when Lachica et
al. (1992) showed that M-recipient layer 4C neurons were
retrogradely labeled after tracer injections in blobs but not
interblobs. Layer 4C neurons were labeled after injections in either
region (but see Yoshioka et al., 1994).
Although these findings suggest a lack of M input to interblobs, there
is other evidence for M input to interblobs. Neuronal activity is
decreased for both blob and interblob neurons after inactivation of
either M or P layers of the LGN (Nealey and Maunsell, 1994), and some
interblob cells are selective for low spatial frequencies (Edwards et
al., 1995), a trait suggestive of M input.
Our aim therefore is to reveal how the type of LGN input to layer 4C
neurons is related to their output to layer 4B and to the blob and
interblob regions of layer 2/3. We have directly assessed these
relationships by reconstructing the axonal and dendritic arbors of
intracellularly labeled layer 4C spiny stellate neurons. The
relationships of their dendritic arbors to layers 4C and 4C
reveal the likely contributions of the M and P pathways to their input.
The patterns of axonal arborization of the same cells reveal their
potential contributions to neurons in more superficial layers.
In addition to identifying neurons with axonal projection patterns
predicted from retrograde labeling studies, we have identified sources
of M input to interblobs and cell types that were not anticipated. As
expected, we found layer 4C cells projecting specifically to blobs
and layer 4B and found layer 4C cells projecting to blobs and
interblobs, but we also found three other cell types in layer 4C.
One cell type has axons restricted to layer 4C, whereas the other two
can provide M input to interblobs. Cells providing M input to
interblobs either have narrowly stratified dendrites restricted to
lower 4C and dense axons specifically targeting layer 3 interblobs,
or they have dendrites in lower 4C and 4C and axons targeting
blobs and interblobs. These findings point out the importance of
considering functional differences between the type of M input to upper
versus lower layer 4C (cf. Blasdel and Lund, 1983).
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MATERIALS AND METHODS |
Twenty-three spiny stellate neurons with somata in layer 4C of
the primary visual cortex of rhesus macaque monkeys were
intracellularly labeled with biocytin, and their axonal and dendritic
arbors were reconstructed. The neurons in our sample were labeled in V1
brain slices prepared from six rhesus macaque monkeys (Macaca
mullata). The ages, sex, and number of cells labeled from each
animal were as follows: (1) 10 months, male, one cell; (2) 13 months,
male, eight cells; (3) 15 months, male, three cells; (4) 15 months, male, four cells; (5) 16 months, female, two cells; (6) 17 months, male, five cells. Other brain slices prepared from the same animals were used for unrelated studies.
The methods used for cell labeling and reconstruction have been
described in detail previously (Callaway and Wiser, 1996; Wiser and
Callaway, 1996; Yabuta and Callaway, 1998). Briefly, living coronal
brain slices were prepared from V1 and held in interface chambers. They
were then transferred to a recording chamber in which whole-cell patch
electrodes were used to record intracellularly from layer 4C neurons
and fill them with biocytin. The slices were then fixed and
double stained for CO to reveal laminar boundaries and CO blobs and
with biocytin to reveal neuronal processes.
Spiny stellate neurons with axonal processes that could be followed to
their ends or until they left the plane of the brain slice without
fading were selected for further analysis. Photographs of a typical
cell are shown in Figure 1. The axonal and dendritic arbors of each
cell were reconstructed using a light microscope with Neurolucida, a
computerized camera lucida system (MicroBright Field Inc.), and a 60×,
1.4 NA oil immersion microscope objective. Synaptic boutons were
identified using a 100× objective when necessary, and their positions
were marked. En passant synaptic boutons were identified as
periodic axonal swellings, and boutons terminaux were
identified as spine-like protrusions with a bulbous ending. Laminar
boundaries revealed by the pattern of CO staining were also identified,
as were the locations of the centers of CO blobs (see Fig. 1). After
neuronal reconstruction, sections were stained for Nissl substance with
thionin to identify the layer 4C/4C border.
Rather than assigning the locations of synaptic boutons to discrete
blob or interblob compartments, our quantitative analyses were based on
the distance of each synaptic bouton to the nearest blob center. The
centers of CO blobs were marked as a straight line running through the
darkest staining region of each blob from layer 1 to layer 4A. The
distances of synaptic boutons from blob centers were calculated as the
shortest distance from each bouton to a point on the line indicating
the nearest blob center.
This method of analysis was chosen because (1) there likely are not
sharp transitions that distinguish blobs from interblobs as discrete
binary entities, and (2) the sizes and spacing of blobs are highly
variable. Because the density of CO staining changes gradually, the
location of any distinct boundary drawn between blobs and interblobs is
necessarily subjective (Edwards et al., 1995). Furthermore, functional
transitions (Livingstone and Hubel, 1984; Edwards et al., 1995) and the
relationships of horizontal connections to blobs (Yabuta and Callaway,
1998) shift gradually with respect to blob centers. Therefore,
describing the distance of synaptic boutons to blob centers is
advantageous, because it provides a more objective description and also
has the potential to reveal any trends in the data that are gradual rather than discrete. For illustrative purposes, we have nevertheless marked transitions from blobs to interblobs in our neuronal reconstructions.
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RESULTS |
Twenty-three spiny stellate neurons with somata in layer 4C were
intracellularly labeled with biocytin in living coronal brain slices
prepared from area V1 of six juvenile rhesus macaque monkeys (M. mullata) (Fig. 1). The axonal and
dendritic arbors of each cell were reconstructed, and the positions of
all synaptic boutons were marked to allow quantitative analyses.
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Figure 1.
Photomicrographs of a section from a V1 brain
slice containing an intracellularly labeled layer 4C spiny stellate
neuron. The section is double stained for biocytin to reveal the
labeled neuron and CO to reveal laminar boundaries and blobs. In the
low-power view to the left, the CO blobs (indicated by
arrows) and laminar pattern of CO staining (layers
indicated by numbers to the left) are
clearly visible. The white boxes outline regions of the
section corresponding to the higher-magnification micrographs shown at
the right. The top box corresponds to the
top right micrograph and the bottom box
to the bottom right micrograph. The top
right micrograph illustrates the densely labeled axonal
processes arborizing in layers 4A and 3B. The bottom
right micrograph illustrates the cell body, dendrites, and
rising axonal processes of the biocytin-labeled neuron. The neuron is
located in lower layer 4C, has narrowly stratified dendrites
confined to lower 4C, and has an axonal arbor specifically targeting
an interblob in layer 3. The reconstruction of this neuron is shown in
Figure 4B. Scale bars: left panel,
200 µm; right panels, 50 µm.
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For descriptive purposes, we divide the 23 labeled cells into groups on
the basis of their cell body positions, patterns of dendritic
arborization, and/or patterns of axonal arborization. We are primarily
interested in the relationships of neurons to input from different
types of LGN afferents. We therefore distinguish three layer 4C zones,
each of which receives different geniculate contributions. Blasdel and
Lund (1983) identified two types of M afferents, one targeting only
upper layer 4C and the other targeting both upper and lower 4C; P
afferents target layer 4C (Hubel and Wiesel, 1972; Hendrickson et
al., 1978). We therefore distinguish upper layer 4C from lower
4C, a narrow zone at the bottom fifth of 4C. Sixteen of the
neurons in our sample have cell bodies in layer 4C: 10 in upper
4C and six in lower 4C. The percentage in lower 4C is higher
than expected by chance, because we explicitly targeted many of our
electrode penetrations to this narrow zone. Seven neurons have somata
in layer 4C.
Upper 4C neurons
Reconstructions of neurons with somata in upper layer 4C are
illustrated in Figures 2 and
3, B and C. We
distinguish two cell types with somata in upper 4C. The most common
cell type at this depth (8 of 10 cells) has axonal arbors projecting to layers 2-4B (Fig. 2). The other type (2 of 10 cells) only rarely extends axons above layer 4C (Fig.
3B,C). Two of the six lower 4C
cells are also of the latter type (Fig. 3A) and will
also be considered here.
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Figure 2.
Reconstructions of the axonal and dendritic arbors
of spiny stellate neurons, with somata in upper layer 4C and axonal
arbors invading the superficial layers (layers 2-4B). All four cells
(A-D) have substantial axonal arbors in layers
4B and 4C and weaker projections to deeper layers. The axonal arbors
of cells A-C extend into layer 3, where they
selectively target blobs. Horizontal lines indicate
laminar boundaries, with the layers identified by the
numbers and letters at the
left of each panel. Vertical
dashed lines indicate blob-interblob transitions, with blobs
marked B and interblobs marked I. Axonal
arbors are indicated by the thinner, more
extensive irregular lines extending from the cell bodies, which
are indicated by the filled, approximately
circular polygons. The axonal arbors are shown in their actual
positions relative to the laminar boundaries and CO blobs. So that
axons and dendrites are not confused, dendritic arbors (thicker
lines emanating from copies of the cell bodies) are shown
shifted to one side from their actual positions. Cell bodies have been
enlarged to make them more visible in the figures. Scale bars, 200 µm.
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Figure 3.
Reconstructions of the axonal and dendritic arbors
of spiny stellate neurons, with somata in lower layer 4C
(A) or upper layer 4C (B,
C) and axonal arbors remaining primarily below layer 4B.
The axonal arbors of these cells are primarily confined to layers 4C
and 6. Cells with dendrites extending into layer 4C have axonal
arbors at the bottom of layer 4C, as well as in layer 4C
(A). Cells with dendrites only in layer 4C
confine their layer 4C axonal arbors to 4C (B,
C). Conventions are the same as in Figure 2. Scale bars,
200 µm.
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Layer 4C cells without axons in superficial layers are distinct from
those projecting to layer 4B and above. For example, the 11 layer 4C
and lower 4C cells in our sample (see below) that project to layers
3B and 4A (and not 4B) all have distinctive rising axon collaterals,
extending nearly vertically above the cell body (Figs.
4, 5). None
of the four cells lacking superficial projections has this type of axon
collateral. Instead, any rising axon collaterals are configured like
those of the upper 4C cells with superficial projections (Fig. 2).
Nevertheless, these cells differ not only in their superficial
projections but also in their projections to deeper layers. Upper layer
4C cells projecting to layers 2-4B usually have axonal branches in
layer 5 (seven of eight cells), while all four cells projecting only as
high as layer 4C clearly lack layer 5 branches (compare Figs. 2 and 3).
Finally, the lack of superficial projections does not result from the
cutting of axon collaterals during slice preparation. With few
exceptions, the rising axons of cells without projections to
superficial layers end within the plane of the brain slice.
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Figure 4.
Reconstructions of the axonal and dendritic arbors
of spiny stellate neurons, with somata in lower layer 4C and axons
extending into layer 3. The cells in A and
B have narrowly stratified dendritic arbors that are
confined to lower 4C and do not extend into upper 4C or 4C.
The axonal arbors of these cells selectively target layer 3 interblobs.
C and D illustrate cells with dendrites
extending into layer 4C. The axonal arbors of these cells target
both blob and interblob regions of layer 3. Conventions are the same as
in Figure 2. Scale bars, 200 µm.
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Figure 5.
Reconstructions of the axonal and dendritic arbors
of spiny stellate neurons, with somata in layer 4C. The axonal
arbors of these cells target both blobs and interblobs in layer 3, regardless of whether their dendrites extend into layer 4C
(A, B) or remain confined to 4C
(C, D). Sparser axonal arbors are present
in layer 4C and occasionally in deeper layers. Conventions are the same
as in Figure 2. Scale bars, 200 µm.
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Although layer 4C cells without superficial projections differ from
other upper 4C cells in their projections to layer 5, both cell
types can have axonal branches in layer 6 (five of eight superficially
projecting cells; two of four cells that lack superficial projections).
Quantitative differences in the laminar distributions of the synaptic
boutons from these cells are illustrated in Figure 6A. The two types of
4C cells (Fig. 6Ai,Aii) provide similar numbers of synaptic boutons per cell within layers 4C and 6, but the
cells with projections to more superficial layers have far more boutons
in layer 5.
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Figure 6.
Histograms illustrating the laminar distributions
(A) and columnar distributions relative to blobs
(B) of synaptic boutons grouped according to five
cell types (i-v): i, upper and lower
layer 4C neurons without axons extending above layer 4C;
ii, upper layer 4C neurons with axons extending above
layer 4C; iii, lower 4C neurons with narrowly
stratified dendrites and layer 3 axons; iv, lower 4C
neurons with dendrites extending into layer 4C and layer 3 axons;
and v, layer 4C neurons. In A, the
synaptic boutons from all cells of a given type were pooled together
and binned according to cortical layers, as indicated to the
left of the histograms. The axes at the
bottom of the histograms indicate the percentages of
boutons from each cell type located within each layer. The
axes at the top of the histograms
indicate the numbers of boutons per cell located within each layer. The
histograms in B illustrate the distributions relative to
blob centers for synapses located within layer 2/3. The
numbers at the bottom of each histogram
indicate the upper limit of distances from blob centers for synapses
counted in that bin. The axes at the left
of the histograms indicate the percentages of boutons from each cell
type located within each range of distances from their nearest blob
center. The axes to the right indicate
the numbers of boutons per cell located in each range of distances from
blob centers.
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Upper layer 4C cells with axonal arbors in layer 3 preferentially
target blobs. In our sample, these projections are provided by seven
upper 4C cells, with projections to both layers 2/3 and 4B (Fig.
2A-C). [One of the eight upper 4C cells with
superficial projections extends axons only to layer 4B (Fig.
2D).] Preferences of axonal arbors for blob regions
are apparent from visual inspection of the reconstructions (Fig.
2A-C). Six of the seven cells with axons in layer 3 have blob preferences similar to those illustrated. The one remaining
cell has axonal arbors in layer 4B and in an interblob zone in layer 3 (data not shown). The axons from this one cell contribute 225 synaptic
boutons to layer 2/3; for comparison, the cell illustrated in Figure
2B has 246 boutons in layer 2/3, and the average for
all seven cells is 283 boutons per cell.
To quantify the overall contributions of these seven cells to blob
versus interblob regions, the distance of every synaptic bouton within
layer 2/3 (1979 boutons from seven cells) to the center of its nearest
blob was measured (see Materials and Methods). These values were
pooled for all seven cells and plotted in the histogram shown in Figure
6Bii. More than half of all layer 2/3 synaptic
boutons from these cells are located within 50 µm of the center of a
blob; more than 80% are within 100 µm. Virtually all of the
remaining boutons are contributed by the cell with axons preferentially
in an interblob (see above), and these account for all of the boutons
in the secondary peak at >200 µm from blob centers.
Lower 4C neurons
Three cell types were distinguished in lower layer 4C. Of six
cells, two have axons that do not extend above layer 4C (Fig. 3A). These cells have been described along with similar
cells in upper 4C (see above). It is noteworthy, however, that these two cells differ from those in upper 4C in that both cells have dendritic branches extending into layer 4C and axonal branches at
the bottom of layer 4C.
The remaining four cells with somata at the bottom of layer 4C have
axons extending through layer 4B and arborizing in layers 4A and 3;
they have only sparse axonal arbors in deeper layers (Fig. 4). Two of
these four cells have narrowly stratified dendritic arbors that do not
extend into layer 4C (Figs. 1,
4A,B). They are therefore likely to
sample input from M afferents that target lower 4C but not from P
afferents or M afferents that target only upper 4C. The axons of
these cells preferentially target layer 3 interblobs. The other two
cells have dendrites in lower 4C, extending into layer 4C. They
are therefore likely to receive P input, as well as input from M
afferents that target lower 4C. Their axons arborize in both blobs
and interblobs (Fig. 4C,D) but not 4B, similar to
the axons of layer 4C spiny stellates (Fig. 5, see below). They
differ from layer 4C cells, because many 4C cells lack dendrites
in layer 4C and therefore cannot sample from M afferents.
Quantitative analyses reveal the relationships between axonal
projections and blobs for both types of lower 4C cells that have
axons extending to layer 2/3. The two cells with stratified dendrites
(Fig. 4A,B) contribute 2132 synaptic boutons to layer 2/3 (1,066 boutons per cell). This is nearly
fourfold more boutons per cell than upper 4C neurons contribute to
layer 2/3. The distribution of boutons is clearly biased toward
distances far from blob centers (Fig. 6Biii). More
than half of the boutons are located >200 µm from a blob center, and
more than 90% are >100 µm away. The two cells with dendrites
extending into layer 4C contribute 1574 synaptic boutons to layer
2/3 (787 per cell), and these are distributed uniformly across blobs
and interblobs (Fig. 6Biv).
4C neurons
All seven layer 4C spiny stellate neurons in our sample have
similar axonal and dendritic morphologies, regardless of the depth of
the cell body within the layer or the distribution of dendrites
relative to the 4C/4C border. The dendrites of cells near the top
of layer 4C frequently cross into lower 4C (Fig. 5A),
whereas cells deeper in 4C restrict their dendrites to 4C (Fig.
5D). No layer 4C cells have dendrites extending into
upper layer 4C. All seven cells have axons that extend through layer 4B and arborize in layers 3 and 4A, without any overall preference for
blob versus interblob regions. Only two of the seven cells have axonal
branches below layer 4C, and these are found in layer 6, not in layer
5. It is noteworthy that compared with layer 4C cells, the 4C
cells contribute similar numbers of boutons per cell within layer 4C,
but these boutons are more evenly distributed between 4C and 4C
rather than focused on 4C (Fig. 6, compare Aii and
Av).
Quantitative analyses of the synaptic boutons within layer 2/3 reveal
their relatively high density and even distribution with respect to
blobs. The layer 4C spiny stellates contribute an average of 1378 layer 2/3 boutons per cell. This is close to five times the average
number of boutons contributed to layer 2/3 by each upper 4C cell.
About half of the layer 2/3 boutons from layer 4C cells are located
within 100 µm of a blob center, and the other half are more distant
(Fig. 6Bv).
Despite the dispersion of the boutons of 4C cells relative to
blobs, their high density leads to a large contribution to both blob
and interblob regions. For example, although upper 4C cells
specifically target blobs in layer 2/3, they contribute a per cell
average of only 230 boutons within 100 µm of blob centers, whereas
4C cells each contribute 700 boutons per cell in the same region.
Furthermore, there are more layer 4C cells than 4C cells
projecting axons to layer 2/3 for each square millimeter of
cortical area (see below) (Beaulieu et al., 1992).
Relative contributions of M- and P-recipient neurons
We have estimated the relative synaptic contributions of each
layer 4C cell type to layers 2/3 and 4B and the distributions of the
layer 2/3 synapses relative to blobs. From these estimates, it is
possible to quantitatively evaluate the contributions of M- versus
P-recipient neurons. It is crucial to be aware that these estimates
should not be considered to be indicative of the relative influences of
the M and P pathways on each of the recipient zones. We are describing
synaptic boutons from layer 4C spiny stellates only; synapses
originating from other cell types, such as layer 4B neurons, also make
substantial contributions with their own specific laminar and columnar
distributions. It should also be kept in mind that not all synapses are
likely to be functionally equivalent; synapses arising from one cell
type might be stronger or weaker than those coming from another cell
type (Stratford et al., 1996).
First, we must estimate the relative proportions of each of the cell
types we have identified, assuming that inherent sampling biases and
small sample sizes have not grossly skewed the sample. We estimate that
approximately half of all layer 4C spiny stellate neurons are located
in layer 4C. This estimate is derived from the observation of
Beaulieu et al. (1992) that there is a 1.4 times higher density of
neurons in the lower versus upper half of layer 4C, combined with the
observation that in our material the cell-dense zone corresponding to
layer 4C is only ~40% of the depth of layer 4C. We next assume
that our small sample of neurons in lower 4C is representative of
one-fifth of all 4C spiny stellate neurons (the region corresponds
to 20% of the thickness of 4C; see above), or 10% of all layer 4C
neurons. The remaining 40% of layer 4C neurons are represented by our
sample of upper 4C neurons.
For each type of layer 4C spiny stellate, what percentage of all layer
4C spiny stellate cells do they constitute? For upper 4C cells,
layer 2/3 boutons are contributed by 70% (7 of 10) of the cells.
Seventy percent times 40% gives 28 as the percentage of all layer 4C
cells represented by this population. Eighty percent of the upper 4C
cells (32% of all layer 4C cells) project to layer 4B. Lower 4C
contains three cell types, which together constitute 10% of layer 4C
cells, or 3.3% for each cell type. The 4C cells all have synaptic
boutons in layers 2/3 and 4B, and these cells are half of all layer 4C
spiny stellates.
We then estimate, for each cell type, the numbers of layer 2/3 and
layer 4B boutons and the distributions of layer 2/3 boutons relative to
blobs, contributed by a "typical" population of 100 layer 4C cells.
For example, to determine the numbers of boutons in layer 4B or layer
2/3 from each cell type, the numbers of boutons per cell in the layer
of interest (Fig. 6A) are multiplied by the weighting
for the cell type (as calculated above). To determine the distributions
of the layer 2/3 synapses from each cell type relative to blobs, the
values are the average numbers of boutons per cell at each distance
from blob centers (Fig. 6B) times the weighting for
each cell type.
Layer 4B input
The overwhelming majority of synapses originating from layer 4C
spiny stellates and terminating in layer 4B come from neurons in upper
layer 4C. We estimate that a population of 100 layer 4C neurons
provides 21,053 synaptic boutons to layer 4B. More than 80% of these
(16,928 boutons, 80.4%) come from neurons in upper layer 4C (529 boutons per cell × 32 cells). Only 3.2% of the synapses come
from lower layer 4C neurons. The remaining 16.4% of the synapses
come from the unbranched axons of layer 4C spiny stellates as they
pass through layer 4B (68.9 boutons per cell × 50 cells = 3445 boutons).
Layer 2/3 input
We estimate that 100 layer 4C spiny stellate neurons contribute
82,914 synapses to layer 2/3. Thus, the population of layer 4C neurons
contributes approximately fourfold more synapses to layer 2/3 than to
layer 4B (82,914 vs 21,053 boutons per 100 layer 4C spiny stellates).
The majority of layer 2/3 synapses that come from layer 4C spiny
stellates are from layer 4C neurons. Layer 4C cells contribute
68,883 (83.1%) of these synapses, which is nearly five times the
remaining number (14,031) contributed by all the layer 4C cell types
combined. Of the synapses contributed to layer 2/3 by layer 4C
cells, (1) upper layer 4C cells contribute 7916 synapses (9.5% of
the layer 2/3 boutons), (2) lower 4C cells with stratified dendrites
contribute 3518 synapses (4.2%), and (3) lower 4C cells with
dendrites in 4C contribute 2597 synapses (3.1%).
The spatial distributions of the layer 2/3 synapses relative to blobs
are illustrated in Figure 7. Figure
7A shows estimated numbers of synaptic boutons contributed
by each cell type from a population of 100 layer 4C spiny stellate
neurons. Figure 7B illustrates the same data, except that
the data in each bin of the histogram are expressed as a
percentage of boutons from that bin only.
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Figure 7.
Histograms illustrating the relative synaptic
contributions of each of four cell types (see legend at
right of B) at various ranges of
distances from blob centers in layer 2/3. In A, the
axis to the right of the histogram
corresponds to the estimated number of synaptic boutons contributed by
a representative population of 100 layer 4C spiny stellate neurons (see
Results). The axis to the left
corresponds to the percentage of all boutons from all 100 cells. In
B, the same bouton distributions are expressed as the
percentage of boutons within each bin (range of distances from blob
centers) of the histogram.
|
|
At all distances from blob centers, layer 4C neurons contribute the
great majority of synapses originating from layer 4C spiny stellate
neurons. The percentage of synapses contributed by the 4C cells is
smallest at the extreme distances, very near to and very far from blob
centers. At >200 µm from blob centers, 4C cells contribute 67%
of the synapses, and at <50 µm, they contribute 75%. These
percentages increase at intermediate distances, peaking at 93% at
100-150 µm from blob centers.
The distribution of synapses contributed by layer 4C cells
complements the 4C cell distribution, peaking very far from blob centers (33% at >200 µm away) and also near to blob centers (25% at <50 µm). Within the population of 4C cells, upper 4C cells contribute most of the synapses near blob centers, whereas lower 4C
cells contribute most of those far from blob centers.
| |
DISCUSSION |
The primate visual system is characterized by parallel pathways.
In the retino-geniculo-cortical pathway, the M and P streams are
distinct and well segregated. Extrastriate cortical areas (beyond V1)
can be separated into a dorsal stream, specialized for analysis of
spatial relationships and object motion, and a ventral stream,
specialized for object identification (Desimone and Ungerlieder, 1989).
The transient responses of M cells seem to be well suited for the
production of motion-sensitive neurons, as found in the dorsal stream,
whereas the small, color-opponent receptive fields of P neurons seem to
be well suited to the later analysis of color and shape required for
object identification in the ventral stream (Livingstone and Hubel,
1988). [A third system, the K stream, may also contribute importantly
to color processing via its input directly to blobs (cf. Livingstone
and Hubel, 1882, 1984; Casagrande, 1994; Hendry and Yoshioka, 1994; Martin et al., 1997).]
At a first approximation, our quantitative data support this notion.
Layer 4B cells project to dorsal visual areas (for review, see Felleman
and Van Essen, 1991), and the great majority of the input from layer 4C
to layer 4B comes from M-recipient layer 4C neurons. Conversely,
layer 3 cells project to ventral visual areas, and the overwhelming
majority of their layer 4C input comes from P-recipient layer 4C neurons.
M and P contributions to layer 3 neurons
Taken at face value, these observations might suggest that the M
pathway has only a minor influence on layer 3, regardless of the
location relative to blobs, but it is important to consider additional
input from sources outside of layer 4C and possible differences in the
functional influence of synapses from different cell types. Layer 4B
neurons receive strong input from the M pathway and have dense axonal
arbors, specifically in layer 2/3 blobs (Callaway and Wiser, 1996).
Although the numbers of synapses from layer 4B cells have not been
quantitatively analyzed, their blob-specific arbors appear similar in
density and blob-specificity to upper 4C neurons. Blob-specific
input to layer 3 also comes from K-type LGN afferents (Casagrande,
1994; Hendry and Yoshioka, 1994). Additional projections to layer 3 arise from neurons in layers 4A, 5, and 6 (Callaway and Wiser, 1996;
Wiser and Callaway, 1996). The contribution from layer 5 is
particularly dense, and we report here that this layer receives input
from the M-recipient layer 4C but not from 4C. Likely, functional
differences in the input from these disparate sources make it still
more difficult to estimate the relative contributions of the M and P
(and K) pathways to layer 3. However, it appears likely that the
influence of the M pathway is greater than suggested by simply counting
synapses. For example, inactivation of M layers of the LGN can
profoundly reduce visual activation of layer 2/3 neurons, irrespective
of their position relative to blobs (Nealey and Maunsell, 1994). The
spatial frequency and contrast sensitivities of neurons in layer 3 blobs are also suggestive of a strong M contribution (Edwards et al.,
1995).
M and P contributions to layer 4B neurons
Just as the relatively strong input from layer 4C to layer 3 should not be taken as an indication that layer 3 lacks M input, one
should not assume that a lack of projections from 4C cells to layer
4B implies that layer 4B cells are not influenced by the P stream.
Photostimulation studies have revealed substantial excitatory synaptic
input from layer 4C neurons onto layer 4B pyramidal cells (Sawatari
and Callaway, 1996). For some cells, there appeared to be as much input
from 4C as from 4C, but in the present study, we find that upper
4C cells provide five times more synapses to layer 4B than 4C
cells. Thus, much of the input from 4C cells onto layer 4B neurons
is likely to be located on apical dendrites of pyramidal neurons. The
surprisingly high density of layer 2/3 synapses that come from layer
4C neurons argues that their synapses onto apical dendrites of layer
4B pyramidal neurons could be numerous. We estimate that 4C cells
contribute four times more synapses to layer 3 than 4C cells
contribute to layer 4B. Synapses localized to apical dendrites might,
however, have a less direct functional influence in vivo,
which is not apparent from the measurement of synaptic responses
in vitro.
M and P contributions to blobs and interblobs
Within layer 2/3, we have further characterized the relationships
of M and P pathways to blob versus interblob regions. The laminar
patterns of dendritic arbors of individual layer 4C spiny stellate
neurons reveal the likely contributions of M and P afferents to their
input. The patterns of axonal arborization relative to extrastriate
projection neurons in the CO blobs and interblobs of layer 2/3 provide
insight into the likely contributions of the same M- and P-recipient
neurons to higher cortical areas.
We find that neurons with dendrites in the upper part of layer 4C
have axonal arbors in layer 4B and the CO blobs of layer 2/3 but rarely
in interblobs, but some neurons, with somata deeper in layer 4C,
lack dendritic branches in upper 4C and provide dense input to CO
interblob regions. The layer 4C spiny stellates providing this
interblob input are of two types: (1) cells with narrowly stratified
dendrites restricted to lower 4C and dense axonal arbors specific
for interblobs; (2) cells with dendritic branches in lower 4C and
4C, whose axons target both blobs and interblobs. Layer 4C spiny
stellates have extremely dense axonal arbors in both blobs and
interblobs but not layer 4B. Some of these 4C neurons have dendritic
branches in lower 4C and can therefore sample M input, as well as P input.
These findings point out the importance of considering possible
subdivisions of layer 4C beyond the traditional 4C-4C
distinction. Most notably, the middle of layer 4C (lower 4C) appears
to play an unique role in visual information processing. This has been emphasized previously by the experimental findings and observations of
Lund and colleagues (cf. Blasdel and Lund, 1983; Mates and Lund, 1983;
Yoshioka et al., 1994). Our findings provide a clearer view of how the
dendritic arbors of individual spiny stellate neurons in this region
are related to their patterns of axonal arborization.
We find that neurons in the bottom of layer 4C make substantial
axonal projections to interblobs. These cells presumably provide M
input to interblobs. Outside of this zone, our reconstructions of
neurons in upper layer 4C and in layer 4C are primarily in keeping with expectations from the retrograde labeling studies of
Lachica et al. (1992) (but see Yoshioka et al., 1994). Upper 4C
neurons provide input to layer 4B and to layer 3 blobs but relatively
little input to interblobs. Layer 4C neurons provide strong
input to blobs and interblobs but much less to layer 4B.
In considering the possibility of M input to interblobs, it is
important to emphasize that layer 4C cells with axons projecting to
interblobs only rarely have dendrites in upper layer 4C. This is a
crucial point, because there appear to be two types of M afferents, one
that targets only upper layer 4C and another that innervates the
whole depth of layer 4C (Blasdel and Lund, 1983). The cells
connecting to interblobs therefore cannot receive input from the subset
of LGN M afferents whose axons only invade upper 4C (Blasdel and
Lund, 1983). Instead, an M contribution to interblobs appears to arise
from the M afferents that target both upper and lower 4C. The 4C
cells specifically targeting blobs and layer 4B, on the other hand, do
have substantial dendritic branches in upper 4C and are therefore
likely to relay input from both types of M afferents. These
observations suggest that both blobs and interblobs receive
contributions from the M pathway, as implied previously by inactivation
studies (Nealy and Maunsell, 1994). This arrangement also helps to
explain why many neurons in interblobs, like blob cells, have
relatively low optimal spatial frequencies, despite the general trend
for higher frequencies farther from blobs (Edwards et al., 1995).
Functional differences between blobs and interblobs appear to be
attributable in part to functional differences between the type
of M input to the two regions rather than a lack of M input to interblobs.
Functional implications
Consideration of the functional differences between the various
types of geniculate afferents is therefore important for interpreting the functional implications of the present findings. The primate retina
and LGN are characterized by many functionally and anatomically distinct types of neurons (for review, see Casagrande and Norton, 1991;
Casagrande, 1994). Prominent among these are the M and P cells, which
constitute the M and P retino-geniculo-cortical pathways. P cells in
the retina and LGN are characterized by color-opponent receptive
fields, sustained visual responses, tuning to high spatial frequencies,
and poor luminance contrast sensitivity. M cells are characterized by a
lack of wavelength selectivity, transient visual responses, tuning to
low spatial frequencies, and high luminance contrast sensitivity. M
cells can be further subdivided based on the linearity of spatial
summation within their receptive fields. Linear M cells (~75% of all
M cells in the LGN) have receptive fields that are remarkably similar
to X cells in the cat and can therefore be referred to as
MX. Nonlinear M cells are like cat Y cells and can be
referred to as MY (Kaplan and Shapley, 1982; Shapley and
Perry, 1986). P cells are linear but otherwise bear relatively little
functional similarity to either X or Y cells in cats.
Because the most striking difference among M cells is the
MX versus MY distinction, it is natural to
guess that this difference correlates with the variation in laminar
specificity of M afferents. We speculate that the M afferents
projecting exclusively to upper layer 4C are of the MY
variety, whereas those projecting throughout 4C are MX.
The basis for this speculation is the possible homology between
MX and MY cells and X and Y cells in the cat.
The remarkable functional similarities between these cell types suggest
that the M-recipient layer 4C in the primate might be organized like layer 4 of the cat. In cat area 17, geniculate Y cells usually innervate just upper layer 4, whereas X cells innervate its entire depth (Ferster and LeVay, 1978; Gilbert and Wiesel, 1979; Humphrey et
al., 1985).
If our speculation is correct, what are the implications? Because we
find that neurons with dendrites in lower 4C project to interblobs
and those with dendrites in upper 4C project to blobs, we suggest
that blobs are influenced by both the MX and MY
pathways, whereas interblobs are influenced by just the linear MX pathway (Fig. 8). Because
the only other input to interblobs would be from layer 4C cells
receiving linear P input, we suggest that interblobs receive only
linear input. Furthermore, neurons receiving exclusively MX
input and no P input (those with narrowly stratified dendrites) provide
output exclusively to interblobs. Thus, any properties unique to these
cells would not be transmitted to blobs or layer 4B. Conversely,
properties unique to upper layer 4C neurons receiving both
MX and MY input would be transmitted to layer
4B and to blobs but not to interblobs (Fig. 8).
View larger version (42K):
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|
Figure 8.
Schematic diagram illustrating four types of layer
4C spiny stellate neurons that project axons to layer 3, the
relationships of their dendritic arbors to M and P afferents from the
LGN, and the relationships of their axonal arbors to laminar boundaries
and to CO blobs in layer 3. The far left of the four
cell types has dendrites confined to layer 4C, where it presumably
receives input from LGN M afferents but not P afferents. We speculate
that such input comes both from MY afferents targeting only
upper layer 4C and MX afferents targeting upper and
lower 4C. The axons of this cell type arborize in layers 4A and 4B
and layer 3 blobs. The next cell type from the left
(middle left) has narrowly stratified dendrites confined
to lower layer 4C. We speculate that it receives input from
MX but not MY or P LGN afferents. The axons of
this cell type arborize preferentially in layer 3 interblobs. The next
cell type (middle right) is located in lower layer 4C
and has dendrites in lower 4C and in 4C. We suggest that these
cells receive input from MX and P afferents but not
MY afferents. The axons of these cells arborize in layer 4A
and layer 3 blobs and interblobs. The last cell type (far
right) is found in layer 4C. These cells either have
dendrites confined to layer 4C and receive just P input (as
illustrated) or also have dendrites extending into lower 4C, where
they might receive MX input. The axons of these cells
arborize in layer 4A and layer 3 blobs and interblobs.
Horizontal lines indicate laminar boundaries, with
layers identified to the left. Darker shaded
regions in layer 2/3 indicate blobs (B),
and lighter regions indicate interblobs
(I).
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These relationships suggest a further similarity between the cat and
monkey systems. In area 17 of cats, blobs receive direct input from
nonlinear Y cells (Shoham et al., 1997). Thus, the two species may have
in common a linear interblob system interrupted by blobs that also
receive nonlinear Y or MY input. Perhaps upper layer 4 in
cats also projects specifically to blobs.
Further studies will be required to gain still greater understanding of
the roles of each type of layer 4C spiny stellate neurons in visual
information processing. In vivo studies correlating receptive field properties to the anatomical properties we have described here would be particularly useful. Similar studies relating the visual responses of LGN neurons to their laminar patterns of axonal
termination in V1 (i.e., upper vs lower 4C) will also provide
significant insight.
| |
FOOTNOTES |
Received July 1, 1998; revised Aug. 24, 1998; accepted Aug. 26, 1998.
This work was supported by National Institutes of Health Grant EY10742.
We thank Jami Dantzker for assistance in labeling neurons and Atomu
Sawatari for tissue processing. Atomu Sawatari and Drs. Amy Butler,
Francis Crick, and Lisa Croner provided valuable comments on earlier
versions of this manuscript.
Correspondence should be addressed to Edward M. Callaway, Systems
Neurobiology Laboratories-C, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037.
| |
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F. Briggs and E. M. Callaway
Layer-Specific Input to Distinct Cell Types in Layer 6 of Monkey Primary Visual Cortex
J. Neurosci.,
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M. L. J. Crawford, R. S. Harwerth, E. L. Smith III, S. Mills, and B. Ewing
Experimental Glaucoma in Primates: Changes in Cytochrome Oxidase Blobs in V1 Cortex
Invest. Ophthalmol. Vis. Sci.,
February 1, 2001;
42(2):
358 - 364.
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N. H. Yabuta, A. K. Butler, and E. M. Callaway
Laminar Specificity of Local Circuits in Barrel Cortex of Ephrin-A5 Knockout Mice
J. Neurosci.,
August 1, 2000;
20(15):
RC88 - RC88.
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Abstract
Introduction
