Department of Psychology, Vanderbilt University, Nashville, TN 37203, USA
Address correspondence to Jon Kaas, Department of Psychology, Vanderbilt University, 301 Wilson Hall, Nashville, TN 37203, USA. Email: jon.kaas{at}vanderbilt.edu.
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Abstract |
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Key Words: extrastriate cortex inferior temporal cortex neuronal tracers posterior parietal cortex primates
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Introduction |
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Materials and Methods |
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Tracer Injections
Surgical procedures were performed under aseptic conditions on monkeys anaesthetized with 2% isoflurane. The dorsolateral visual cortex was exposed and injections of different fluorescent dyes 3% Fast Blue (FB), 2% Diamidino Yellow (DY), 10% Fluororuby (FR) and 10% Fluoroemerald (FE) in distilled water as well as 2% wheatgerm agglutinin conjugated to horseradish peroxidase (WGA-HRP; Sigma Chemicals) and 1% cholera toxin-subunit B (CTB; Sigma Chemicals) in distilled water or 10% solution of biotinylated dextran amine (BDA; Molecular Probes) in phosphate buffer were made with a micropipette coupled to a Hamilton syringe. Injections of 0.51 µl of fluorescent dyes, BDA or CTB and 0.05 µl of WGA-HRP were placed in several locations in the dorsolateral visual cortex just rostral to the lunate and inferior occipital sulci and caudal to the superior temporal sulcus (Fig. 1). The most dorsal injection was between the tip of superior temporal sulcus (STS) and intraparietal sulcus, and the most ventral injection was just rostral and ventral to the lower bank of the inferior occipital sulcus. Other injections were distributed along the prelunate gyrus. Injections were placed 11.5 mm deep into the cortex to avoid damage and uptake of tracers by underlying fibers. All injection locations and extents were later verified in the prepared histological material.
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After 710 days of survival (or 5 days in case 99-36 when WGA-HRP was injected), monkeys were administered a lethal dose of sodium pentobarbital and perfused intracardially with warm phosphate buffered saline followed by fixative (2% paraformaldehyde and then 2% paraformaldehyde with 10% sucrose), and their brains were removed. The posterior part of the cortex, from the lateral sulcus backward was carefully separated from the rest of the brain, and sulci were unfolded (Fig. 2). The cortex was flattened by gentle pressure between two glass slides and placed in 30% sucrose in buffered saline overnight for cryoprotection (see Krubitzer and Kaas, 1990). The next day, the cortex was cut parallel to the cortical surface into 40- or 50-µm-thick frozen sections. Sections were separated into five series. A set of unprocessed sections was mounted for examination of fluorochromes, and other series of sections were processed to reveal BDA (in case 98-66), BDA/CTB (in case 00-51) or WGA-HRP/CTB (in case 99-36). Processing procedures for BDA, BDA/CTB and WGA-HRP and CTB follow those described elsewhere (Sakai et al., 2000
; Stepniewska et al., 2003
). In each case, an additional series of sections was processed for myelin (Gallyas, 1979
) or cytochrome oxidase (CO) (Wong-Riley, 1979
) to reveal the architecture of cortical regions.
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Neurons labeled with fluorescent tracers were plotted at high resolution under ultraviolet illumination with a Leitz microscope coupled to an XY plotter (Igor Pro 3.14, Wave Metrics, Inc.). Neurons labeled with WGA-HRP and CTB were plotted under dark (WGA-HRP) or bright field (CTB) illumination with a Wild microscope with a drawing tube attached. For each case the injection sites and label were drawn from individual sections, which were superimposed with adjacent sections using blood vessels and other landmarks for local alignment, and the final drawing was prepared. Patterns of connections were related to architectonic boundaries in adjacent sections processed for myelinated fibers or cytochrome oxidase. Composite images of the reconstructions were created using Canvas v.8.0 software installed on a Power Mac G4 computer. The final drawings were analyzed to reveal the connection pattern resulting from each tracer injection. The connection patterns from injections in similar and dissimilar locations were compared to determine differences and consistencies across injection sites and cases. The symbols used in the final drawings demarcate the proportions and locations of labeled cells, but underestimate their actual number for simplicity.
Identification of Cortical Areas and Boundaries
Interpretations of the connection patterns in the present cases were greatly aided by the identification of the boundaries of several visual areas by architectonic criteria as reference areas, and the estimation of the locations and extents of other areas based on widely accepted depictions. In our processed brain sections of flattened visual cortex, we were able to reliably identify three visual areas that are components of all current proposals of visual cortex organization (for a review, see Kaas and Lyon, 2001). V1 was easily identified and delineated in both CO and myelin preparations due to the pattern of dark CO blobs and CO and myelin dense middle cortical layers, V2 was obvious over much of its extent as a result of its pattern of alternating CO dark and CO light bands, and MT was clearly visible as a CO and myelin dark oval (for photomicrographs, see Stepniewska and Kaas, 1996
). The boundaries of other visual areas were largely or completely estimated from previous descriptions. The position of V3 was based on the recent description of Lyon and Kaas (2002)
. In part, V3 was also identified in favorable sections by thicker but less obvious CO bands than in V2 (Lyon and Kaas, 2002
). The location of the dorsomedial visual area, DM, corresponds to that estimated from V1 connection patterns and myeloarchitecture (Lyon and Kaas, 2002
). In the present material, DM also appeared darker than adjoining areas in CO and myelin preparations, but borders were somewhat uncertain. The dorsolateral visual complex, DL, consists of rostral and caudal divisions with similar but somewhat different connections (see Discussion). The borders of these two areas were based on our earlier description (Stepniewska and Kaas, 1996
). DLc is somewhat more densely myelinated than DLr, and this difference was apparent in some of our brain sections. Cortex ventral to DL was considered to be inferotemporal cortex, and rostral (ITr) and caudal (ITc) divisions (Weller and Kaas, 1987
) were denoted without an attempt to mark a boundary between the two. Much of ITc could be included in TEO of previous reports (e.g. Boussaoud et al., 1991
), and the dorsal part of ITc could be included in V4 (see Discussion). The location of the middle superior temporal (MST) area was approximated based on the description by Desimone and Ungerleider (1986)
. As a moderately myelinated area, MST could sometimes be visualized in our sections. The fundal superior temporal area (FST) is estimated from the report of Desimone and Ungerleider (1986)
. Dorsal (FSTd) and ventral (FSTv) portions are distinguished as they have different connections (Kaas and Morel, 1993
). This region is also moderately myelinated. A narrow stripe of cortex along the outer boundary of MT, the MT crescent (MTc) of Kaas and Morel (1993)
was faintly apparent as a band of myelinated patches. Cortex between the dorsal end of the superior temporal sulcus and the intraparietal sulcus is designated ventral posterior parietal cortex (VPP). This region of cortex has been variously included in area 7a and the dorsal prelunate area (DP), or given other terms (for a review, see Lewis and Van Essen, 2000
). Several subdivisions of the cortex of intraparietal sulcus have been proposed, but we only approximate locations of the lateral (LIP), ventral (VIP) and posterior (PIP) intraparietal areas (see Lewis and Van Essen, 2000
).
The locations of areas in the prefrontal cortex were made in reference to the previous architectonic study of Preuss and Goldman-Rakic (1991). We use the numbers of Walker (1940)
for fields largely to aid discussion, and have not attempted to define boundaries.
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Results |
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Connection Patterns in Visual Cortex
Here we briefly describe the connection patterns produced by the 15 injection locations in the four monkeys illustrated in Figures 36. All injections were limited to gray matter, and the white matter revealed by myelin staining in the deep sections was not contaminated by the tracers. In monkey 99-36 (Fig. 3), several closely spaced injections of fluoroemerald (FE) were placed in dorsolateral prelunate cortex in a location that corresponds to the dorsal half of DLc of our terminology (e.g. Stepniewska and Kaas, 1996
), and V4 of basically all V4 descriptions (see Discussion). The injection was just dorsal to the presumptive representation of the zero horizontal meridian, judged to course from the rostral peak of V1 to the ventral margin of MT, and was thus somewhat within the representation of the lower visual quadrant in dorsal DL or V4 as defined by Gattass et al. (1988)
. The location of the injection was approximately the same as injections in caudal V4 of macaque monkeys by Shipp and Zeki (1985)
and DeYoe and Van Essen (1985)
. These two groups of investigators found that their injections labeled neurons in a sequence of bands in dorsal V2 that largely correspond with the thin CO stripes and interstripes of V2 (see also Zeki and Shipp, 1989
). Likewise, our dorsal DL injections labeled a sequence of bands in dorsal V2 representing the visual hemifield from
2° to 4° (Gattass et al., 1981
). Such V2 connections are expected to be an identifying feature of classically defined V4 (Zeki, 1971
). A few labeled neurons appeared to be in retinotopically mismatched locations in ventral V2. Our injections in dorsal DLc also labeled neurons over much of the dorsal DLc and dorsal DLr, and even the ventral DLr. The more widespread pattern in DLr provides further support for considering the two regions as separate areas (see Stepniewska and Kaas, 1996
). Other labeled neurons were in dorsal V3, and more sparsely in retinotopically mismatched ventral V3. Labeled neurons were largely within ventrocaudal MT, corresponding to paracentral vision of the lower visual quadrant, with fewer neurons in ventrorostral MT, corresponding to paracentral vision of the upper visual quadrant (Gattass and Gross, 1981
). Labeled neurons were also in the MTc region, and in ITr of the temporal lobe. A few labeled cells were in ITc, FST and the cortex rostral to FST within the superior temporal sulcus. The connections with the IT cortex are consistent with the evidence that such connections are another defining feature of V4 (e.g. Shipp and Zeki, 1995
; Felleman et al., 1997b
). The separate regions of labeled neurons in ITr and ITc suggest that these are functionally distinct regions, and they also identify regions of temporal cortex that are unlikely to be parts of V4.
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The injection of CTB in case 99-36 was judged from the connection pattern to be just ventral to DLr (Fig. 3). This injection failed to label the targets that define V4. Thus, no labeled neurons were detected in V2 or MT. However, labeled neurons were found in ventral V3, suggesting that the injection was in a part of IT that represents the upper visual quadrant. This could also account for the labeled cells that were judged to be in the ventral extreme of DLr, providing evidence for DLr projections to the temporal cortex. A small focus of label in dorsal DLr would appear to represent retinotopically mismatched connections. Other labeled neurons were widely scattered over ITr and ITc, the visual cortex of the medial wall, and FST and the adjoining cortex in the caudal bank of the superior temporal sulcus.
Injections of tracers in five different locations in case 98-66 further identified the connection pattern of DLc (caudal V4) and the boundaries of DL/V4 (Fig. 4). An injection of FE into a dorsal portion of DLc was similar in location to the DLc injection of the previous case, but smaller in extent. Thus fewer cells were labeled. However, V2, V3 and MT were again labeled, although only a few labeled neurons were in V3. The locations of these labeled neurons in V2, V3 and MT all corresponded to parts representing the central few degrees of the lower visual quadrant. As central V4 has been described as having inputs from central V1 (Zeki, 1978; Nakamura et al., 1993
), it was not surprising to find a few labeled neurons in V1 corresponding to central vision of the lower quadrant near the representation of the vertical meridian. Other labeled neurons were in dorsal DLc, in dorsal and ventral, but mainly ventral, DLr (a retinotopic mismatch) and in ITr cortex.
The other four injection sites in case 98-66 (Fig. 4) helped define the dorsal and ventral boundaries of DL/V4. Injections of BDA and FB in the VPP region were clearly well dorsal to DL, and they labeled neurons in the VPP region, the intraparietal sulcus (possibly VIP, LIP and especially PIP), the visual cortex of the medial wall and the locations of MST in the superior temporal sulcus. An injection of DY was judged to be largely dorsal to DL, but involving the dorsal border of DLc. Thus, there was some label in dorsal V2 in a portion representing 30° into the lower visual quadrant (Gattass et al., 1981
). As the label was along the V1/V2 border, the injection site likely involved the representation of the vertical meridian. Microelectrode recordings have identified neurons with receptive fields on the vertical meridian (Youakim et al., 2001
) in this region of the cortex where V4 is postulated to adjoin a dorsal prelunate visual area termed DP (Maguire and Baizer, 1984
; Van Essen, 1985
; Andersen et al., 1990
). A few clumps of labeled cells were in V1 and others were in caudomedial MT, where the paracentral and peripheral lower visual quadrant is represented. Other labeled neurons were in rostral DM, MST, dorsal DLr, several locations in ITr, scattered locations in the occipito-temporal sulcus and visual cortex of the medial wall, as well as in the region of the frontal eye field (Fig. 7). The connections with cortex of the medial wall identify the injection location as largely outside of DL (Andersen et al., 1990
).
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In case 00-51 injections were placed in central DL, near the dorsal border of DL, and dorsal to DL in the dorsal prelunate (DP) region (Fig. 5). The injection of CTB was judged to include the representation of central vision along zero horizontal meridian in DLc. This injection labeled neurons in portions of dorsal and ventral V1, V2, V3 and MT representing central vision, as well as central and ventral parts of DLr. Other label was in several locations in the IT cortex. All of these connections conform to those expected from central DLc (V4). While the FR injections in case 00-51 would be placed by current estimates in the DP region well dorsal to V4, some neurons were labeled in dorsal V2. As we did not find labeled cells in V2 in other cases with injections in the DP region, it seems unlikely that this cortex is part of V4. Instead, we conclude that DP injections may sometimes label a few scattered neurons in dorsal V2. The FR injection also labeled some neurons along the dorsal border of DLc, a few in dorsal MT and a few groups of cells in the IT cortex in and near the occipito-temporal sulcus. Other labeled neurons were densely distributed in the parietal and intraparietal cortex near the injections, and in the regions of DM and M. More laterally, an injection of BDA near the presumed dorsal border of DLc labeled a similar distribution of neurons, with more neurons labeled in DLc and DLr, possibly as a result of the injection slightly involving DLc.
In a fourth case, 98-102, injections were placed dorsal to DL in DP, at the expected dorsal border of DL and at the expected ventral border of DL (Fig. 6). None of the injections labeled neurons in a pattern that is characteristic of DL/V4, consistent with our judgement that the locations of the injections were largely or completely outside DL. However, the CTB injection did label some neurons near the extreme dorsal end of V2. Cortex in this location could be area prostriata, which borders part of V1 representing peripheral vision (see Rosa, 1997). The injections of DY near the dorsal border of DLc failed to label neurons in V2 or V3, and only a single clump of neurons was found in MT. Other labeled neurons were in the DP and VPP regions, the dorsal extents of DLc and DLr, and ITr, with a few cells in DM and the superior temporal sulcus. The FE injection near the ventral border of DLr failed to label neurons in V2, V3 and MT. Thus, the injection did not appear to involve DL. A few labeled neurons next to the injection site may have been in DL. Other labeled neurons distant from the injection site were in separate IT locations. As the injection site was small, it may not have revealed the complete connection pattern
Connection Patterns in the Frontal Cortex
Some of the injections in the present cases labeled neurons in prefrontal cortex (Fig. 7) in the region of the frontal eye field in the arcuate sulcus (areas 8Am and 45), and in the cortex 8Ar and cortex of the principal sulcus (46d and 46v). Thus, injections in DP that appeared to extend into dorsal DLc (cases 98-66 and 98-102) labeled patches of neurons in 8Am and 8Ar, but injections in central DLc (00-51) did not. However, some of the injections dorsal and ventral to DL labeled neurons in the frontal lobe. Injections in ITc just ventral to DLr labeled neurons in areas 45 and 8Ar (98-66; 99-36, Fig. 7), while injections in VPP and DP labeled neurons in 8Am and area 46 (98-102; 00-51; 99-36; Fig. 7). Thus, injections of tracers into posterior parietal cortex and inferior temporal cortex labeled separate locations in the prefrontal cortex.
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Discussion |
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The V4 region of the visual cortex is also called the dorsolateral visual area, DL, after an early microelectrode mapping study demonstrated systematic representation of the contralateral visual hemifield in the cortex between V2 and MT of New World owl monkeys (Allman and Kaas, 1974b). Here we refer to the region as the DL/V4 complex. In both New World and Old World monkeys there is considerable evidence that the DL/V4 region contains at least three visual areas that parallel each other in visuotopic organization: the MT crescent (MTc) or V4 transitional (V4t), in cortex that borders MT, the adjacent rostral division of DL (DLr) or V4A, and a caudal division of DL (DLc) or V4 proper (for a review, see Stepniewska and Kaas, 1996
). All three areas represent the contralateral visual hemifield from lower quadrant to upper quadrant in a dorsoventral sequence. Because neurons in these areas have relatively large receptive fields and there is considerable receptive fields scatter, microelectrode mapping studies have provided weaker evidence for the three fields than studies of differences in connection patterns. Many investigators include the territories of V4A and V4 within the single representation, V4. As an added complication, Shipp and Zeki (1995)
redefined V4A from part of V4 to much of TEO (see Zeki, 1996
).
There are also uncertainties over the extents of the three areas. V4t has been described as a lightly myelinated area bordering only the portion of MT representing the lower visual quadrant (Desimone and Ungerleider, 1986), thus representing only the lower quadrant, while MTc has been described as a more extensive complete representation (Kaas and Morel, 1993
). The V4 region, when considered as a single area, has been portrayed as having various extents (Fig. 8), especially in its ventral extension into the temporal lobe. The principle goal of the present study was to compare connection patterns of regions of the cortex well within DL/V4 with those possibly outside of DL/V4 to see if similarities and differences in connection patterns could help to define the borders of the complex. The defining differences between DLr (V4A) and DLc (V4 proper) connections are not considered here, but the two related fields share many connections, including V2 and V3 (see Stepniewska and Kaas, 1996
).
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The Connections of DLc/V4
Injections that were well centered in DL (DLc) labeled neurons in V2, V3, MT, IT, other parts of the DL complex and sometimes V1 (Fig. 9). The major connections were those commonly described for DL/V4. In particular, the injections labeled band-like arrays of neurons in V2 that are known from previous studies to project to DL/V4 (De Yoe and Van Essen, 1985; Shipp and Zeki, 1985
; Weller and Kaas, 1985
; Cusick and Kaas, 1988
; Zeki and Shipp, 1989
; Nakamura et al., 1993
; Felleman et al., 1997b
; Xiao et al., 1999
). V2 projects to both divisions of the complex (DLr/V4A and DLc/V4), as originally described by Zeki (Zeki, 1971
), but in different, parallel retinotopic patterns. The connections with DLr are less dense and the representation is more compressed (Stepniewska and Kaas, 1996
). V2 has connections with other regions of extrastriate cortex (e.g. Gattass et al., 1997
), including the IT (TEO) region (Zeki, 1971
) that appears to have been partly included in the expanded version of V4 (Zeki, 1996
; for a review, see Stepniewska and Kaas, 1996
). V3 connections with DL/V4 are less firmly established due to difficulties in defining V3 (Kaas and Lyon, 2001
), but such connections have been described (for a review, see Felleman et al., 1997a
) since the original report of Zeki (1971)
.
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Connections of the DL/V4 region with the IT or TEO region of the temporal lobe are well established (e.g. Zeki, 1977; Seltzer and Pandya, 1978
; Rockland and Pandya, 1979
; Desimone et al., 1980
; Weller and Kaas, 1985
; Weller and Steele, 1992
; Distler et al., 1993
; Felleman et al., 1997b
). Connections of V1 with DL/V4 have been described, but they appear to be variable in magnitude and largely from foveal V1 (Allman and Kaas, 1974a
; Zeki, 1978
; Van Essen et al., 1986
; Nakamura et al., 1993
; for a review, see Casagrande and Kaas, 1994
). Connections of other parts of V1 with DL/V4 have been also described, and V1 has some connections with the IT cortex (e.g. Lyon and Kaas, 2002
). DL/V4 has not been considered as having significant connections with the frontal eye field (Schall et al., 1995
), but a small patch of label was found in the anterior bank of the inferior arcuate sulcus (area 45) after large injections in V4 representing the lower quadrant of the central visual field in a study by Ungerleider et al. (1989)
. Label after an injection involving the DL/V4 border with DP in two of our cases also raises the possibility of connections between DL/V4 and the frontal eye-field (Fig. 7).
Connections of Cortex Near or Beyond the Dorsal Border of DL/V4
We placed different tracers at a total of nine different sites just rostral to the lunate sulcus that were judged to be near the dorsal border of most depictions of V4 or clearly dorsal to that border (Fig. 1). Cortex dorsal to V4 on the exposed brain surface is generally divided into a dorsal prelunate region that adjoins V4 (area DP of Maguire and Baizer, 1984 and Asanuma et al., 1985
) and the nearby caudal extension of area 7a (e.g. Andersen et al., 1990
; Felleman and Van Essen, 1991
), which we have labeled ventral posterior parietal cortex, VPP (Figs 36
). Neither of these regions constitutes a well-defined area of cortex, but the connections of both regions have been studied. Our injections in VPP (7a) were in the more caudal portion that Pandya and Seltzer (1982)
defined as area Opt. The injections labeled the cortical region around the injection sites, cortex in the intraparietal sulcus (LIP, PIP), the DP region, MST, the more distant cortex on the medial wall of the cerebral hemisphere, the region of the frontal eye field, and the cortex of the principal sulcus of the frontal lobe (Fig. 9). Previously, Andersen et al. (1990)
described connections of the caudal portion of area 7a as largely with DP and LIP. Other connections were with MST and the parietal occipital area (PO), which Colby et al. (1988)
considered to be the same as the previously defined medial area M (Allman and Kaas, 1976
). Our more caudal VPP injections (Figs 5 and 6) labeled both of these regions. As in the present study, connections with area 8a and 46 of the frontal lobe were previously noted (Andersen et al., 1990
; Schall et al., 1995
). As the connections of the 7a region have been described in a number of other reports, including studies with lesions or injections in 7a and studies labeling 7a after injections in other areas, a number of proposed visual areas have been related to area 7a (for a review, see Andersen et al., 1990
). Our VPP injections labeled the regions most consistently described as having connections with caudal 7a. None of the current schematics of cortical organization (Fig. 8) include the 7a region of cortex in V4 or the DL complex, and the distinctively different connection patterns of 7a and DL/V4 support this conclusion.
Other injections in the prelunate cortex were either centered in DP or along the expected border of DP with DL (Stepniewska and Kaas, 1996). Injections centered in DP (FR, Fig. 3) labeled neurons throughout DP and in adjoining VPP (7a), DM, PIP, LIP, IT and cortex of the medial wall (Fig. 9). Andersen et al. (1990)
reported a similar connection pattern of DP, including 7a, V3A (DM), LIP (but not PIP), as in the present study, but also V4, MST and PO(m). Connections with the medial wall and IT cortex were not reported (but see Zhong and Rockland, 2003
). However, a slightly more lateral injection in DP (FR, Fig. 5) did label neurons in the M (PO), MST and dorsal DLc (V4) regions, thus including a few more of the targets that Andersen et al. (1990)
reported for DP. Again, neurons were labeled in IT and the cortex of the medial wall, and a few neurons were labeled in dorsal V2, suggesting that these areas have connections with parts of DP, although such connections have been previously unreported. Other described connections of the DP region with VP (V3v) (Van Essen, 1985
) were not seen in our two cases with central DP injections.
Injections near or on the DP/DL (V4) border labeled neurons in parts of dorsocaudal MT and dorsal V2 that represents peripheral vision of the lower visual quadrant, as did a dorsal DL injection, while labeling locations throughout DP, and DP targets such as the intraparietal cortex, DM and MST. We took this mixed pattern of connections as evidence that injection sites included bordering parts of DP and DL/V4. Thus, the injections of DY in case 98-66 (Fig. 4), BDA in case 00-51 (Fig. 5) and DY in case 98-102 (Fig. 6) all appear to define the locations of the DPDL (V4) border. This border corresponds well to our previous estimate of its location based on V2 connections (Stepniewska and Kaas, 1996). The dorsal border of DL/V4 based on present results closely approximates or is somewhat ventral to other current estimates of this border (Fig. 8). The present evidence suggests that DL/V4 does not extend all the way to the dorsal end of the superior temporal sulcus, as in some proposals, but only to a location just ventral to the dorsal end. The present location corresponds to a proposed dorsal boundary of V4 where microelectrode recordings revealed a representation of the zero vertical meridian (Youakim et al., 2001
; also see Maguire and Baizer, 1984
). However, in a previous study where injections were placed in dorsal V4 and possibly in DP, a difference in connection patterns was not noted (Tanaka et al., 1990
).
Connections of Cortex Near the DL/V4IT Border
Our three injections near the DLr and ITc (TEO) border (Figs 3, 4 and 6) all appeared to be mainly in ITc, while slightly involving DLr in two of the cases (Figs 4 and 6). All injections labeled neurons in scattered locations across IT cortex and a few neurons across the border into the ventral tip of DLr (Fig. 9). One case (Fig. 3) also labeled neurons in V3v, FSTd, and cortex caudally adjacent to FSTd, while another case (Fig. 4) also labeled neurons in DLc, FSTv and cortex adjacent to FST. A few neurons were labeled along the ventral V2V1 border. Because none of the injections labeled neurons in rostral MT, representing the upper visual quadrant as does ventral DL/V4, and only one injection labeled any cells in V2v, the injection sites were judged to be completely or nearly completely ventral to DL/V4. As the three injection sites were located rostral to the lip of the inferior occipital sulcus, the injection sites likely define the dorsal border of IT with DLr (original V4A) rather than DLc (V4 proper). Thus, DLc (V4 proper), but not DLr, may extend further into the inferior occipital sulcus. A much greater ventral extent of DLc did not seem likely in our previous estimates based on assumptions about the total V2 projection pattern (Stepniewska and Kaas, 1996), but projections from ventral V2 to cortex as ventral as the occipito-temporal sulcus have been described as belonging to V4 (Gattass et al., 1997
). As these most ventral connections appear to conform to a single retinotopic pattern, they are unlikely to be a part of the weak V2 connections with IT (Zeki, 1971
; Stepniewska and Kaas, 1996
). Previously, large injections in the ITc region have extensively labeled the V4 (DL) region and other parts of the temporal lobe, with weak labeling of parts of V2 and V3 (Morel and Bullier, 1990
; Baizer et al., 1991
; Weller and Steele, 1992
; Distler et al., 1993
; Webster et al., 1994
). Moreover, injections of ITc in previous and present studies labeled prefrontal areas 8 and 45 within the frontal eye-field (Ungerleider et al., 1989
; Webster et al., 1994
; Schall et al., 1995
).
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Conclusions |
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Second, differences in connection patterns provided strong evidence for the dorsal and rostroventral limits of the DL/V4 complex. The results indicate that neither DLr nor DLc extend dorsally much past the level of the dorsal tip of MT, and even more clearly they do not extend to the dorsal tip of the superior temporal sulcus. This conclusion is consistent with a number of previous observations. Differences in connection patterns revealed by ventral injection sites provided evidence for a ventral limit of DLr with ITc (TEO). The results support the conclusion that the dorsal and ventral halves of DLr, divided by a line of foveal vision extending from foveal V1 to foveal MT and representing the upper visual quadrant ventrally and the lower visual quadrant dorsally, are approximately equal in size. Thus, there is no overrepresentation of the upper visual quadrant in DLr. While the results did not define the ventral limit of DLc, they did establish a width of DLc of 8 mm from the border of V3v to the rostral lip of the inferior occipital sulcus. Our previous study of V2 connections with DLc (Stepniewska and Kaas, 1996
) revealed a symmetrical pattern of representations in the dorsal and ventral portions, and suggested a ventral extent of DLc only slightly (5 mm) past the ventral extent of DLr. However, a more extensive study of the projection patterns of V2 (Gattass et al., 1997
) provided evidence for a much more ventral extension, and a disproportionately large upper field representation. While no other interpretation of the Gattass et al. (1997)
data is obvious, the disproportionate representation of the upper field in DLcV4 seems improbable from a functional point of view, and further studies may yet identify part of the V4v region as belonging to another area.
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Acknowledgments |
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References |
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Allman JM, Kaas JH (1974b) A crescent-shaped cortical visual area surrounding the middle temporal area (MT) in the owl monkey (Aotus trivirgatus). Brain Res 81:199213.[CrossRef][ISI][Medline]
Allman JM, Kaas JH (1976) Representation of the visual field in the medial wall of the occipitalparietal cortex in the owl monkey. Science 191:572576.[ISI][Medline]
Allman JM, Jeo R, Sereno, M (1994) The functional organization of visual cortex in owl monkey. In: Aotus: the owl monkey (Baer JF, Weller RE, Kakoma I, eds), pp. 287320. Orlando, FL: Academic Press.
Andersen RA, Asanuma C, Essick G, Siegel R (1990) Cortico-cortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule. J Comp Neurol 286:65113.
Asanuma C, Andersen RA, Cowan WM (1985) The thalamic relations of the caudal inferior parietal lobule and the lateral prefrontal cortex in monkeys. Divergent cortical projections from cell clusters in the medial pulvinar nucleus. J Comp Neurol 241:357381.
Baizer JS, Ungerleider LG, Desimone R (1991) Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaque. J Neurosci 11:168190.[Abstract]
Beck PD, Kaas, JH (1999) Cortical connections of the dorsomedial visual area in Old World macaque monkeys. J Comp Neurol 406:487502.[CrossRef][ISI][Medline]
Boussaoud D, Ungerleider LG, Desimone R (1990) Pathways for motion analysis; cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque. J Comp Neurol 296:462495.[ISI][Medline]
Boussaoud D, Desimone R, Ungerleider LG (1991) Visual topography of area TEO in the macaque. J Comp Neurol 306:554575.[CrossRef][ISI][Medline]
Casagrande VA, Kaas JH (1994) The afferent, intrinsic, and efferent connections of primary visual cortex in primates. In: Cerebral cortex (Peters A, Rockland KS, eds), vol. 10, pp. 201259. New York: Plenum Press.
Colby CL, Gattass R, Olson CR, Gross CG (1988) Topographical organization of cortical afferents to extrastriate area PO in the macaque: a dual tracer study. J Comp Neurol 269:392413.[CrossRef][ISI][Medline]
Cusick CG, Kaas JH (1988) Cortical connections of area 18 and dorsolateral visual cortex in squirrel monkeys. Vis Neurosci 1:211237.[ISI][Medline]
Desimone R, Ungerleider LG (1986) Multiple visual areas in the caudal superior temporal sulcus of the macaque. J Comp Neurol 248:164189.[CrossRef][ISI][Medline]
Desimone R, Ungerleider LG (1989) Neural mechanisms of visual processing in monkeys. In: Handbook of neuropsychology (Boller F, Grafman J, eds), pp. 267299. Amsterdam: Elsevier.
Desimone R, Fleming J, Gross CG (1980) Prestriate afferents to inferior temporal cortex: an HRP study. Brain Res 184:4155.[CrossRef][ISI][Medline]
DeYoe EA, Van Essen DC (1985) Segregation of efferent connections and receptive field properties in visual area V2 of the macaque. Nature 317:5861.[CrossRef][ISI][Medline]
Distler C, Boussaoud D, Desimone R, Ungerleider LG (1993) Cortical connections of inferior temporal area TEO in macaque monkeys. J Comp Neurol 334:125150.[CrossRef][ISI][Medline]
Felleman DJ, Van Essen DC (1983) The connections of area V4 of macaque extrastriate cortex. Soc Neurosci Abstr 10:933.
Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in primate cerebral cortex. Cereb Cortex 1:147.[Abstract]
Felleman DJ, Burkhalter A, Van Essen DC (1997a) Cortical connections of areas V3 and VP of macaque monkey extrastriate visual cortex. J Comp Neurol 379:2147.[CrossRef][ISI][Medline]
Felleman DJ, Xiao Y, McClendon E (1997b) Modular organization of occipito-temporal pathways: cortical connections between visual area 4 and visual area 2 and posterior inferotemporal ventral area in macaque monkeys. J Neurosci 17:31853200.
Fize D, Vanduffel W, Nelisse K, Denys K, Chef d'Hotel C, Faugeras O, Orban GA (2003) The retinotopic organization of primate dorsal V4 and surrounding areas: a functional magnetic resonance imaging study in awake monkeys. J Neurosci 23:73957406.
Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203209.[Medline]
Gattass R, Gross CG (1981) Visual topography of the striate projection zone in the posterior superior temporal sulcus (MT) of the macaque. J Neurophysiol 46:521538.
Gattass R, Gross CG, Sandel JH (1981) Visual topography of V2 in the macaque. J Comp Neurol 21:519539.[CrossRef]
Gattass R, Sousa APB, Gross CG (1988) Visuotopic organization and extent of V3 and V4 of the macaque. J Neurosci 8:18311845.[Abstract]
Gattass R, Sousa APB, Mishkin M, Ungerleider LG (1997) Cortical projections of area V2 in the macaque. Cereb Cortex 7:110129.[Abstract]
Kaas JH (1993) The organization of visual cortex in primates: problems, conclusions, and the use of comparative studies in understanding the human brain. In: The functional organization of the human visual cortex (Gulyas B, Ottoson D, Roland PE, eds), pp. 111. Oxford: Pergamon Press.
Kaas JH, Lyon DC (2001) Visual cortex organization in primates: theories of V3 and adjoining visual areas. Prog Brain Res 134:285295.[ISI][Medline]
Kaas JH, Morel A (1993) Connections of visual areas of the upper temporal lobe of owl monkeys: the MT crescent and dorsal and ventral subdivisions of FST. J Neurosci 13:534546.[Abstract]
Krubitzer LA, Kaas JH (1990) Cortical connections of MT in four species of primates: areal, modular, and retinotopic patterns. Vis Neurosci 5:165204.[ISI][Medline]
Krubitzer LA, Kaas JH (1993) The dorsomedial visual areaof owl monkeys; connections, myeloarchitecture, and homologiesin other primates. J Comp Neurol 334:497528.[CrossRef][ISI][Medline]
Lewis JW, Van Essen DC (2000) Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. J Comp Neurol 428:79111.[CrossRef][ISI][Medline]
Lyon DC, Kaas JH (2002) Evidence for a modified V3 with dorsal and ventral halves in macaque monkeys. Neuron 33:453461.[CrossRef][ISI][Medline]
Maguire WM, Baizer JS (1984) Visuotopic organization of the prelunate gyrus in the rhesus monkey. J Neurosci 4:16901704.[Abstract]
Maunsell JHR, Van Essen DC (1983) The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J Neurosci 12:25632586.
Morecraft RJ, Rockland KS, Van Hosen GW (2000) Localization of area prostriata and its projection to the cingulated motor cortex in the rhesus monkey. Cereb Cortex 10:192203
Morel A, Bullier J (1990) Anatomical segregation of two cortical visual pathways in the macaque monkey. Vis Neurosci 4:555578.[ISI][Medline]
Nakamura M, Gattas R, Desimone R, Ungerleider LG (1993) The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques. J Neurosci 13:36813691.[Abstract]
Pandya DN, Seltzer B (1982) Intrinsic connections and architectonics of posterior parietal cortex in the ehesus monkey. J Comp Neurol 204:196210.[CrossRef][ISI][Medline]
Pinon MC, Gattass R, Sousa AP (1998) Area V4 in Cebus monkey: extent and visuotopic organization. Cereb Cortex 8:685701.[Abstract]
Preuss TM, Goldman-Rakic PS (1991) Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthyropoid primate Macaca. J Comp Neurol 310:429474[CrossRef][ISI][Medline]
Rockland KS, Pandya DN (1979) Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res 179:320.[CrossRef][ISI][Medline]
Rosa MGP (1997) Visuotopic organization of primate extrastriate cortex.. In: Cerebral cortex. Vol. 12. Extrastriate cortex in primates (Rockland KS, Kaas JH, Peters A, eds), pp. 127203. New York: Plenum Press.
Sakai ST, Stepniewska I, Qi H-X, Kaas JH (2000) Pallidal and cerebellar afferents to pre-supplementary motor area thalamocortical neurons in the owl monkey: a multiple labeling study. J Comp Neurol 417:164180.[CrossRef][ISI][Medline]
Schall JD, Morel A, King DJ, Bullier J (1995) Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams. J Neurosci 15:44644487.[Abstract]
Seltzer B, Pandya DN (1978) Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Res 149:124.[CrossRef][ISI][Medline]
Sereno MI, Allman JM (1990) Cortical visual areas in mammals. In: Vision and visual dysfunction. Vol. 4. The neural basis of visual function (Leventhal AG, ed.), pp. 160172: London: Macmillan.
Shipp S, Zeki S (1985) Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature 315:322325.[CrossRef][ISI][Medline]
Shipp S, Zeki S (1995) Segregation and convergence of specialized pathways in macaque monkey visual cortex. J Anat 187:547562.[ISI][Medline]
Stepniewska I, Kaas JH (1996) Topographic patterns of V2 cortical connections in macaque monkeys. J Comp Neurol 371:129152.[CrossRef][ISI][Medline]
Stepniewska I, Sakai ST, Qi H-X, Kaas JH (2003) Somatosensory input to the ventrolateral thalamic region (VL) in the macaque monkeys: a potential substrate for parkinsonian tremor. J Comp Neurol 455:378395.[CrossRef][ISI][Medline]
Tanaka M, Lindsley E, Lausmann S, Creutzfeldt OD (1990) Afferent connections of the prelunate visual association cortex (areas V4 and DP). Anat Embryol 181:1930.[ISI][Medline]
Ungerleider LG, Desimone R (1986) Cortical connections of visual area MT in the macaque. J Comp Neurol 248:147163.[CrossRef][ISI][Medline]
Ungerleider LG, Gattass R, Sousa APB, Mishkin M (1983) Projections of area V2 in the macaque. Soc Neurosci Abstr 9:152.
Ungerleider LG, Gaffan D, Pelak VS (1989) Projections from inferior temporal cortex of prefrontal cortex via the uncinate fscicle in rhesus monkeys. Exp Brain Res 76:473484.[CrossRef][ISI][Medline]
Van Essen DC (1985) Functional organization of primate visual cortex. In: Cerebral cortex (Jones EG, Peters, A, eds), vol. 3, pp. 259329. New York: Plenum Press.
Van Essen DC, Maunsell JHR (1983) Hierarchical organization and functional streams in the visual cortex. Trends Neurosci 6:370375.[CrossRef][ISI]
Van Essen DC, Zeki SM (1978) The topographical organization of rhesus monkey prestriate cortex. J Physiol 277:193226.[Abstract]
Van Essen DC, Newsome VT, Maunsell JHR, Bixby JL (1986) The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: assymetries, areal boundaries, and patchy connections. J Comp Neurol 244:451480.[CrossRef][ISI][Medline]
Vogt BA, Pandya DN (1987) Cingulate cortex of the rhesus monkey. II. Cortical afferents. J Comp Neurol 262:271289.[CrossRef][ISI][Medline]
Walker AE (1940) A cytoarchitectural study of the prefrontal area of the macaque monkey. J Comp Neurol 73:5986.[CrossRef]
Webster MJ, Bachevalier J, Ungerleider LG (1994) Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb Cortex 5:470483.[ISI][Medline]
Weller RE, Kaas JH (1985) Cortical projections of the dorsolateral visual area in owl monkeys: the prestriate relay to inferior temporal cortex. J Comp Neurol 234:3559.[CrossRef][ISI][Medline]
Weller RE, Kaas JH (1987) Subdivisions and connections of inferior temporal cortex in owl monkeys. J Comp Neurol 256:137172.[CrossRef][ISI][Medline]
Weller RE, Steele GE (1992) Cortical connections of subdivisions of inferior temporal cortex in squirrel monkeys. J Comp Neurol 324:3766.[CrossRef][ISI][Medline]
Weller RE, Wall JT, Kaas JH (1984) Cortical connections of the middle temporal visual area (MT) in the superior temporal sulcus in owl monkeys. J Comp Neurol 228:81104.[CrossRef][ISI][Medline]
Wong-Riley M. (1979) Changes in the visual system of monocularly sutured as enucleated cats emonstrable with cytochrome-oxidase histochemistry. Brain Res 171:1128.[CrossRef][ISI][Medline]
Xiao Y, Zych A, Felleman DJ (1999) Segregation and convergence of functionally defined V2 thin stripe and interstripe compartment projections to area V4 of macaques. Cereb Cortex 9:792804.
Youakim M, Bender DB, Baizer JS (2001) Vertical meridian representation on the prelunate gyrus in area V4 of macaque. Brain Res Bull 56:93100.[CrossRef][ISI][Medline]
Zeki SM (1971) Cortical projections from two prestriate areas in the monkey. Brain Res 34:1935.[CrossRef][ISI][Medline]
Zeki SM (1977) Colour coding in the superior temporal sulcus of rhesus monkey visual cortex. Proc R Soc Lond B 197:195223.[ISI][Medline]
Zeki SM (1978) The cortical projections of foveal striate cortex in the rhesus monkey. J Physiol 277:227244.[Abstract]
Zeki S (1996) Are areas TEO and PIT of monkey visual cortex wholly distinct from the fourth visual complex (V4 complex)? Proc R Soc Lond B 263:15391544.[ISI][Medline]
Zeki S, Shipp S (1989) Modular connections between areas V2 and V4 of macaque monkey visual cortex. Eur J Neurosci 1:494506.[ISI][Medline]
Zhong YM, Rockland KS (2003) Inferior parietal lobule projections to anterior inferotemporal cortex (area TE) in macaque monkey. Cereb Cortex 13:527540.