Subcortical connections of area V4 in the macaque

Abstract

Area V4 has numerous, topographically organized connections with multiple cortical areas, some of which are important for spatially organized visual processing, and others which seem important for spatial attention. Although the topographic organization of V4's connections with other cortical areas has been established, the detailed topography of its connections with subcortical areas is unclear. We therefore injected retrograde and anterograde tracers in different topographical regions of V4 in nine macaques to determine the organization of its subcortical connections. The injection sites included representations ranging from the fovea to far peripheral eccentricities in both the upper and lower visual fields. The topographically organized connections of V4 included bidirectional connections with four subdivisions of the pulvinar, two subdivisions of the claustrum, and the interlaminar portions of the lateral geniculate nucleus, and efferent projections to the superficial and intermediate layers of the superior colliculus, the thalamic reticular nucleus, and the caudate nucleus. All of these structures have a possible role in spatial attention. The nontopographic, or converging, connections included bidirectional connections with the lateral nucleus of the amygdala, afferent inputs from the dorsal raphe, median raphe, locus coeruleus, ventral tegmentum and nucleus basalis of Meynert, and efferent projections to the putamen. Any role of these structures in attention may be less spatially specific.

Keywords: amygdala; caudate; claustrum; pulvinar; putamen; superior colliculus.

Figure 1

Photomicrograph of a coronal section of a representative case illustrating an injection into area V4, on the prelunate gyrus. See text for details.

Figure 2

Injection sites in V4 shown in a flattened map of extrastriate cortex. Tracers were placed in 21 injections sites at central and peripheral locations in V4, in nine animals (cases) in 10 hemispheres. Each injection site is numbered and colored to match data from other figures. Myeloarchitectonic borders of visual areas are indicated with dashed lines. The injections from the individual cases were plotted on this map to best retain their locations relative to myeloarchitectonic borders and sulci. For names of areas and sulci, see abbreviations.

Figure 3

Connections of V4 with claustrum, amygdala, putamen, caudate, and pulvinar in a photomontage of parasagittal sections of Case 6p. Retrograde labeled cells (red-orange concentric icons) and/or terminals (blue dots) were found in each subcortical structure after injection of HRP in V4. Five parasagittal sections were cut, aligned, and staked to reconstruct most of the extent of the claustrum. An inset of section #50 shows the projection in the putamen (lower left), while another inset of section #62 shows the projections in caudate and in the different projection zones of the pulvinar (lower right). Two patches of labeled cells were found in in ventral (VC) and mid (MC) claustrum; three patches were found at corresponding topographical locations in P1, P2, P3, and P4 in the pulvinar; one patch in the putamen; one patch in the lateral basal (lb) nucleus of the amygdala and another in the caudate nucleus. For names of nuclei, see abbreviations.

Figure 4

Representative coronal sections stained for Nissl through the rostral-to-caudal (top-to-bottom) extent of the pulvinar. Left: cytoarchitectonic subdivisions, according to Olszewski (1952). Right: the pulvinar fields, P1, P2, P3, and P4, are shown superimposed on each section. Solid circles indicate the representation of the vertical meridian, solid squares indicate the representation of the horizontal meridian, heavy dashes indicate isoeccentricity lines, gray colored dashes indicate isoeccentricity lines in areas of coarse topography, small solid triangles indicate the borders of P3 and P4, and small dotted lines indicate the borders of the pulvinar fields. The plus sign indicates the upper visual field representation and the minus sign indicates the lower visual field representation. The sections are spaced 0.5 mm apart, and they do not reach the caudal extent of the pulvinar. For names of nuclei, see abbreviations. Scale bars = 1 mm.

Figure 5

Photomicrograph of the pulvinar and surrounding areas showing the projections from V4 in Case 4p. Three patches of silver grains were found at corresponding topographic locations in P2, P3, and P4 of the pulvinar; one patch was found in the thalamic reticular nucleus (RN) and two additional patches were found in the caudate nucleus (Cd).

Figure 6

Connections of pulvinar with V4 in Cases 2, 3, and 5. Two or three anterograde and retrograde tracers were injected at topographical locations (right) in V4 as illustrated in the lateral view of the hemisphere. Labeled cells and terminals are shown in coronal sections through the pulvinar and surrounding areas (left). For details see text.

Figure 7

Four topographically organized projection fields (P1–P4) of the pulvinar revealed after injections of tracers in V4 at the eccentricities shown in eight selected cases (left). A–D: Reconstructions of coronal sections of the pulvinar from anterior (A) to posterior (D) regions. Representations of the topographic maps in the four projection zones of the pulvinar are drawn at four coronal sections through the pulvinar (right).

Figure 8

Connections of the claustrum to and from area V4. Afferent and efferent connections of V4 to the claustrum are shown in coronal sections at the level indicated in the lateral reconstruction of the claustrum in four selected cases. The projections of one lateral reconstruction of the claustrum onto the lateral reconstruction of the hemisphere are shown in gray (center).

Figure 9

Two topographically organized areas in the claustrum: vCL (blue) and mCL (red). (+), representation of the upper visual field; (–), representation of the lower visual field in the areas of the claustrum.

Figure 10

Nontopographic connections to the lateral basal nucleus of the amygdale (lb). Cells (circle) and terminals (+) in the dorsal part of the amygdala after HRP injections in V4 are shown in one coronal section in two representative colors.

Figure 11

Projections to the putamen. Labeled terminals were found in different topographical locations in the putamen. A: superimposition of projection zones all animals (left) segregated in upper and lower field projections (right) B: coronal sections through the putamen in three animals. The locations of these cells are shown in the lateral reconstructions (C). The labeled cells are located in the posterior portion of the putamen in all animals as illustrated in the enlarged view (D) of the posterior portion of the putamen.

Figure 12

Projections to the caudate nucleus. The entire projection of V4 to the caudate nucleus (gray areas) in all animals encompasses most of the caudate, except for the most anterior portions of the head and the tail of the nucleus. The reconstructions of the projections in the caudate are shown on the representation of the lateral and dorsal hemispheres (top). The projection zones were superimposed onto the lateral and dorsal reconstructions of the caudate (middle) and onto coronal section through the caudate nuclei (bottom).

Figure 13

Projections to the caudate nucleus in Cases 2, 8, and 5. Terminals were found in the caudate nuclei after injections of two anterograde tracers in V4. The levels of the coronal sections (upper left) are indicated by vertical lines in the reconstructions of the caudate. In the enlarged sections (upper right) of the caudate nuclei, the location of terminals are shown after injections of ³H-amino acids and HRP at different topographical locations. The labels are also shown in the lateral (left) and dorsal (right) reconstructions of the caudate nucleus.

Figure 14

Topographically organized projections of the V4 to the superficial layers of the superior colliculus in six cases. Coronal (Cases 1–5) and oblique (Case 8) sections of the superior colliculus show topographically organized projections, after injection of one or two anterograde tracers in V4. The visuotopic locations of the injections sites are shown in the representation of the contralateral visual hemifield (lower right) and the reconstruction of the projection zones are shown on the superior colliculus surface (lower left).

Figure 15

V4’s subcortical connections can be segregated into visutopically organized (blue) and non-visuotopically organized ones (yellow). Topographical gates (and efferents) allow spatial attention filtering of the information leading to the timporal lobe. Together these structures could act as topographically distributed networks, enhancing or facilitating visual processing at specific loci in V4.