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Previous Article | Next Article
The Journal of Neuroscience, July 1, 2000, 20(13):5083-5101
Connections between Anterior Inferotemporal Cortex and Superior Temporal Sulcus Regions in the Macaque Monkey
K. S. Saleem1, 2, W. Suzuki1, 3, K. Tanaka1, 4, and T. Hashikawa1 1 Riken Brain Science Institute, Wako, Saitama 351-0198, Japan, 2 Brain Science and Life Technology Research Foundation, Wako, Saitama 351-0198, Japan, 3 Graduate School of Engineering Sciences, Osaka University, Toyonaka, Osaka 560-0043, Japan, and 4 Core Research for Evolutional Science and Technology, Japan Science and Technology Corporation, Wako, Saitama 351-0198, Japan
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
We examined the connections between the anterior inferotemporal cortex and the superior temporal sulcus (STS) in the macaque monkey by injecting Phaseolus vulgaris leucoagglutinin (PHA-L) or wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) into the dorsoanterior and ventroanterior subdivisions of TE (TEad and TEav, respectively) and observing the labeled terminals and cell bodies in STS. We found a clear dichotomy in the connections of the rostral part of STS: the injections into TEad resulted in a dense distribution of labeled terminals and cell bodies in the upper bank of rostral STS, whereas labeling was confined to the lower bank and fundus of rostral STS after injections into TEav. The distribution of labeling in the rostral STS was discontinuous from the distribution of labeling surrounding the injection sites: the lower bank of the rostral STS was spared from labeling in the TEad injection cases, and TEad had only sparse distribution in the TEav injection cases. These results revise the classical view that the lower bank of rostral STS is connected with TE, whereas the upper bank of rostral STS is connected with the parietal, prefrontal, and superior temporal regions (Seltzer and Pandya, 1978
, 1991
Key words: inferotemporal cortex; area TE; superior temporal sulcus; polysensory area; PHA-L; WGA-HRP; laminar organization; macaque monkey
INTRODUCTION
Inferotemporal area TE of the macaque monkey is an extrastriate visual cortical area that represents the final purely visual stage in the occipitotemporal pathway (Gross, 1994
It has recently been found that the dorsal and ventral subregions of anterior TE (TEad and TEav, respectively) differentially project to the perirhinal and entorhinal cortices (Saleem and Tanaka, 1996
In the present study we examined connections of TEad and TEav with the superior temporal sulcus (STS). Both connectional and physiological studies have shown that the upper bank and fundus of STS are polymodal, whereas the lower bank of STS is purely visual (Seltzer and Pandya, 1978
Some of the present results have been reported previously in abstract form (Saleem et al., 1996
MATERIALS AND METHODS
Eleven Japanese monkeys (Macaca fuscata) of both sexes, weighing between 3.3 and 6.9 kg, were used. PHA-L was injected into the TEad in one monkey and the TEav in two other monkeys. WGA-HRP was injected into the TEad in another two monkeys, the TEav in another three monkeys, at the border between the TEav and area 36 of the perirhinal cortex in another monkey, and in area 36 in another monkey. In addition, WGA-HRP was injected into the superior temporal polysensory area (STP) in the upper bank of rostral STS in the last monkey, to confirm the connections of STP with TEad and the absence of STP connections with TEav. The tracers were injected into a single site except in the STP injection case, in which WGA-HRP was injected into two nearby sites to cover a larger part of STP. Some of these cases are shared with other studies conducted in our laboratories (Saleem and Tanaka, 1996
Surgery and tracer injection. The tracers were injected during aseptic surgery under general anesthesia, as described previously (Saleem and Tanaka, 1996
STS and the anterior middle temporal sulcus (AMTS) were exposed after craniotomy to use as landmarks for placement of injection site. PHA-L (2.5%; Vector Laboratories, Burlingame, CA) was injected iontophoretically (Midgard precision current source, Stoelting) according to the procedure recommended by Gerfen and Sawchenko (1984)
Histological processing. Two days after the WGA-HRP injection and 16-18 d after the PHA-L injections, the monkey received a lethal dose of sodium pentobarbital (60-80 mg/kg, i.v.) and was perfused transcardially with 1 l of 0.9% warm heparinized saline, followed by 3-4 l of cold 4% paraformaldehyde in 0.1 M phosphate buffer, pH 7.2-7.4, then 1-2 l of 10% sucrose in 0.1 M phosphate buffer, and finally by 1 l of 20% sucrose in 0.1 M phosphate buffer. The flow rate of the fixative solution was adjusted so that the perfusion with paraformaldehyde took 30-45 min. The brain was immediately removed from the skull, blocked, photographed, and then stored in 30% buffered sucrose at 4°C until it sank. Frozen sections were cut in the coronal plane at 35 or 40 µm in the PHA-L cases and at 50 µm in the WGA-HRP cases. All sections were processed in the PHA-L cases, whereas a series of every fifth section was processed in the WGA-HRP cases. The remaining sections in the latter cases were stained for Nissl and parvalbumin to determine the cortical areal and laminar borders. Some of the PHA-L sections were also stained for Nissl after the PHA-L observation was completed, to determine the cortical areal and laminar borders. Transported PHA-L was visualized by the same procedure as that described in Saleem et al. (1993)
Data analysis. The sections were observed with a light microscope under bright- and dark-field illumination. To examine the global distribution of labeling, labeled terminals and cell bodies in STS, TEO, and TE were first plotted onto enlarged camera lucida drawings of sections, which were later transformed into two-dimensional unfolded maps. Sections were usually sampled at 0.5 mm intervals in the WGA-HRP cases to make the unfolded maps, and the sampling interval was decreased to 0.25 mm when the distribution of labeling was sparse. In the PHA-L cases, sections were sampled at 0.42 or 0.48 mm intervals to make the unfolded maps. To examine the laminar distribution of labeling, the PHA-L-labeled terminals were observed with a 10× objective lens in all the sections containing labeling, and the labeled terminals were plotted with a camera lucida in every 4th-12th section (140-420 µm).
In PHA-L cases, most of the labeled segments were axon terminals with synaptic boutons, especially in the regions with dense labeling. Axon segments without boutons were observed around the border between the white matter and layer 6 but constituted only a small percentage of the labeled segments within the clustering of labeling in the gray matter.
Unfolded map. A series of coronal sections encompassing the full rostrocaudal extent of STS, TE, and TEO (Fig. 1A) were drawn using camera lucida. Layer IV was then traced on these drawings using Nomarsky optics or from adjacent Nissl- and parvalbumin-stained sections. The middle point of the fundus and the upper and lower lips of STS were marked on these camera lucida drawings (Fig. 1B, right). The absolute distances from the middle point of the fundus to the upper and lower lips of STS were measured in each section using a digital curvimeter placed over layer IV. The layer IV contour lines were straightened, and the positions of the upper and lower lips of STS were marked on the straight lines. These straight contour outlines were then aligned in parallel to produce a two-dimensional unfolded map of the entire STS (Fig. 1B, middle). The outline of STS served as reference points in the arrangement of the sections; i.e., the middle points of the fundus were aligned along the shape of STS taken from the photograph of the lateral view of the brain (Fig. 1B, top left). The other sulci, the AMTS, posterior middle temporal sulcus (PMTS), rhinal sulcus (RS), and occipitotemporal sulcus (OTS), were also unfolded. The absolute distances between the sulci were maintained along the vertical contour lines in the unfolded map. Because the contour lines were not stretched or shrunken in the unfolding process, the distortion of cortical area is minimal in and around STS and larger at positions near the rhinal sulcus and occipitotemporal sulcus. The unfolded maps dorsally cover cortical regions up to the dorsal lip of STS, except Figure 15, where more dorsal regions are covered up to the ventral lip of the sylvian fissure (SF). The ventral limits of the unfolded maps are the medial lips of the rhinal sulcus and occipitotemporal sulcus. The parahippocampal gyrus and the medial part of the entorhinal cortex are not shown in the unfolded maps.
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Figure 1. A, Lateral (top) and ventral (bottom) views of the right hemisphere showing the location and extent of the TEad and TEav, perirhinal cortex (areas 35 and 36), and the parahippocampal gyrus (TF/TH). Area 35 is located in the fundus of rhinal sulcus. B, Reconstruction of two-dimensional unfolded map, in which the superior temporal sulcus (sts), anterior middle temporal sulcus (amts), posterior middle temporal sulcus (pmts), occipitotemporal sulcus (ots), and rhinal sulcus (rs) are exposed. The solid lines indicate the lips and fundi of the sulci, and the broken lines show the borders between cortical areas. As opposed to conventional unfolding, the coronal sections are represented by vertical straight lines in the unfolded map. Camera lucida drawings of three representative coronal sections are shown on the right (sections 16, 44, and 68). The broken lines in the coronal sections indicate the borders of layer 4. The arrows indicate the borders between different cortical areas. HC, Hippocampus; C, caudal; R, rostral; D, dorsal; V, ventral.
The labeling was projected to layer 4 along the axes of cortical columns within the coronal sections and plotted on the unfolded maps. Because the cortical columns in the dorsal and ventral banks of STS are rostrally or caudally tilted from the coronal sections, there remains some misalignment. The points in the upper and lower layers within a single column are plotted to different positions on the unfolded map, which are rostrocaudally displaced, but because the angle between the STS and horizontal plane was up to 45° given the cortical thickness of 2.5 mm, this misalignment is estimated to be <1.8 mm.
Nomenclature. There are several different proposals for subdividing TE in macaques based on cytoarchitectonic, connectional, or behavioral criteria (Seltzer and Pandya, 1978
Our definition of the border between TEav and the perirhinal cortex is similar to that of Amaral and colleagues (Suzuki and Amaral, 1994
Seltzer and Pandya (1978)
RESULTS
Injection sites
The PHA-L and WGA-HRP injections into TEad and TEav were well localized within TEad or TEav. The injection sites in the TEad cases were located at the middle between the lower lip of STS and the lateral lip of the anterior middle temporal sulcus (Figs. 2A, 3-5), whereas the injections sites in the TEav cases were located at the medial lip of the anterior middle temporal sulcus (Figs. 2B, 8-11). In the case in which WGA-HRP was injected at the border between TEav and area 36 (Figs. 2C, 13; TEav/36 border case), the injection did not cover the medial part of area 36 located within the rhinal sulcus. In the case in which WGA-HRP was injected into the caudal part of area 36 (Figs. 2D, 14), the injection covered the lateral lip of the rhinal sulcus, and its lateral border was ~1.5 mm medial to the TEav/36 border. The PHA-L injections were circumscribed to small foci, which were 0.5-1.0 mm in width in the plane parallel to the cortical layers. They included all of the cortical layers, except in one TEad case (Fig. 5, case 3) in which the injection was restricted to layers 3-6. The WGA-HRP injections were larger (1.5-3.0 mm in width) and included all the cortical layers. Note that the shape of the injections in the flattened maps does not represent their exact shape because of distortion by the flattening procedure.
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Figure 2. Photomicrographs illustrating the WGA-HRP injection sites in TEad (A), TEav (B), at the border between TEav and area 36 of the perirhinal cortex (C), and in area 36 (D). The positions of these injection sites are schematically illustrated in the coronal section drawing at the top right. For the PHA-L injection sites, see Saleem and Tanaka (1996)
TEad Cases
In all three TEad injection cases, the labeling in STS was mainly found in two groups of clusters; one in the upper bank of the rostral STS and the other in the lower bank and fundus of the rostrocaudally middle part of STS. The two groups of clusters do not overlap each other along the rostrocaudal axis. In the WGA-HRP cases, the distribution of retrogradely labeled cell bodies roughly coincided with that of anterogradely labeled terminals in the plane parallel to the cortical surface. There was no cluster in STS that contained only labeled terminals or cell bodies in the TEad cases.
The distribution of labeling in the upper bank of the rostral STS was composed of two clusters in case 1 (Fig. 3) and one cluster in case 2 (Fig. 4). They occupied the middle depth of the upper bank, which mostly overlapped with TPO of Seltzer and Pandya (1978)
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Figure 3. Distribution of labeled terminals and cell bodies in the two-dimensional unfolded map (left) and three representative coronal sections (right) after a WGA-HRP injection into TEad (case: 1). The darkest black region in the unfolded map and the lateral view of the brain indicate the extent of injection, whereas the gray regions indicate the distribution of labeled terminals and cell bodies. The darkness of the gray indicates the density of the distribution. The rostrocaudal levels of the illustrated coronal sections are indicated in the unfolded map as well as in the lateral view of the brain. The distribution of labeled terminals and cell bodies in the circumscribed regions in coronal sections (57 and 82) are shown in the dark-field photomicrographs in Figure 7, A and B. The brain regions posterior to the vertical lines in the unfolded map were not examined. Two groups of labeled terminals and cell bodies were found in STS: one group in the upper bank of the rostral STS and the other in the lower bank and fundus of the rostrocaudally middle part of STS. All other conventions are as in Figure 1.
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Figure 4. Distribution of labeled terminals and cell bodies after a WGA-HRP injection into TEad (case: 2). The rostrocaudal extent of the examined coronal sections is indicated by the broken lines in the lateral view of the brain. All other conventions are the same as in Figure 3.
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Figure 5. Distribution of anterogradely labeled terminals after a small PHA-L injection into TEad (case: 3). The gray shading in the unfolded map indicates the distribution of labeled terminals. The segments in the coronal sections represent labeled terminals and axon segments. The small filled region in the coronal section 661 indicates the PHA-L injection site. Other conventions are as in Figure 3.
The labeled terminals in the upper bank of the rostral STS were distributed in all the cortical layers (Figs. 3 and 7A, section 82; Fig. 6, section 680) or were found predominantly in layers 1-3 (Fig. 4, section 54; Fig. 6, sections 664 and 672) in both WGA-HRP and PHA-L cases. The concentrations of labeled terminals in layer 2 and the upper part of layer 3 were the highest in the PHA-L case, whereas the quantitative comparison of labeled terminal concentrations was difficult in the WGA-HRP cases. The concentrations of labeled terminals in layer 1 were not higher than those in layer 2 and the upper part of layer 3. Cell bodies retrogradely labeled in the WGA-HRP cases were found equally in layers 2-3 and 5-6 (Figs. 3, 7A, section 82) or were restricted to layers 5-6. The confined distribution of labeled cell bodies in layers 5-6 was found in more rostral parts within the clusters.
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Figure 6. High magnification camera lucida drawings of patchy regions in STS that show the laminar distribution of PHA-L-labeled terminals in case 3. Top, Patches obtained from the upper bank of rostral STS (STP; sections 664, 672, and 680); bottom, a patch obtained from the lower bank of rostrocaudally middle STS (section 448). The positions of the patches are indicated by the gray shading in the coronal section drawings and by the rectangular boxes in the unfolded map.
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Figure 7. Dark-field photomicrographs showing the laminar distribution of labeled terminals and cell bodies in the rostral STS (A, C) and the posterior regions (B, D) after WGA-HRP injection into TEad (A, B, case 1) and TEav (C, D, case 4). A, A patch in section 82 obtained from the upper bank of the rostral STS (shown in Fig. 3); B, a patch in section 57 from the lower bank of the middle STS (shown in Fig. 3); C, a patch in section 84 from the lower bank of the rostral STS (shown in Fig. 8); D, two patches, one in section 32 and the other in section 33, obtained from the lateral lips of the occipitotemporal sulcus (shown in Fig. 8). Scale bars: A-C, 0.25 mm; D, 0.5 mm.
The distribution of labeling in the lower bank and fundus of the rostrocaudally middle part of STS was composed of multiple clusters. Some of them were very elongated (Figs. 3, 5), whereas others had complex shapes (Fig. 4). Only a part of the elongation of clustering can be explained by the misalignment caused by the oblique cutting of cortical columns (see the Materials and Methods). Their exact positions along the rostrocaudal axis varied among the cases. They were located mostly at the TEp level in case 1 (Fig. 3), mostly at the TEO level in case 3 (Fig. 5), and around the borders between the TEp and TEO levels in case 2 (Fig. 4). The clusters in the fundus extended to the deepest part of the upper bank in all three cases. Therefore, it may be said that the distribution of labeling in the upper bank of STS was composed of two groups: one in the rostral STS and the other in the middle STS. We do not favor this interpretation because the cluster in the middle STS was always located at the deepest part of the upper bank, whereas the cluster in the rostral STS was located at the middle or shallow part of the upper bank. The distribution in case 3 (Fig. 5) partially invaded FST in the fundus, but otherwise no labeling was found in MT, MST, FST, and V4t located in the caudal part of STS.
In WGA-HRP and PHA-L cases, the labeled terminals in the lower bank and fundus of the middle STS were distributed in both layers 1-3 and 5-6 (Figs. 3, 7B, section 57; Fig. 6, section 448), predominantly in layers 1-3 (Fig. 4, section 16; Fig. 5, section 481), or predominantly in layers 5-6 (Fig. 5, section 421). Layer 4 had none or only sparse distribution of labeled terminals. The concentrations of labeled terminals in layer 1 were as high or higher than those in layers 2 and 3. Retrogradely labeled cell bodies in the WGA-HRP cases were found in layers 2-3 and 5-6, with the densest distribution in layer 3B (Fig. 7B). The labeled cell bodies in layers 2-3 appeared in dense clusters, whereas those in layers 5-6 were more evenly distributed (Fig. 7B).
Sparse labeling was observed in a small cluster in TEpd in case 1 (Fig. 3), and in an elongated cluster encompassing both TEO and TEpd in cases 2 and 3 (Figs. 4, 5). In all the cases, these distributions on the lateral surface were much less extensive than those in the adjoining regions in the lower bank of middle STS. The labeling resulting from the intrinsic connections around the injection sites was extensive in all three cases, but they invaded the lower bank of STS only minimally. None of the cases showed labeling in TEpv or the ventral part of TEO.
TEav cases
True of all five TEav injection cases, the distribution of labeling in STS was limited to the lower bank and fundus of the rostral half of the sulcus. No labeling was found in the more caudal parts of STS. In the WGA-HRP cases, the distribution of retrogradely labeled cell bodies roughly coincided with that of anterogradely labeled terminals in the plane parallel to the cortical surface.
There was some variation in the detailed pattern of labeling distribution in the lower bank and fundus of STS. The distribution in cases 4 and 8 was composed of one large cluster, which extended in the lower bank of the rostral half of STS (Fig. 8) (case 8 is not shown). The rostrocaudal levels of the clusters corresponded to TEad and the anterior half of TEpd but did not invade TG. The distribution in cases 5, 6, and 7 was composed of two clusters (Figs. 9-11). One cluster, which was larger than the other, was located at the rostral end of STS and invaded TG in all three cases. The other, smaller cluster was located at the rostrocaudal level corresponding to TEpd in cases 5 and 7 (Figs. 9, 11) and the border between TEpd and TEad in case 6 (Fig. 10). The distribution of labeling slightly invaded the upper bank of STS in cases 6 and 7 (Figs. 10, 11), but not in cases 4, 5, and 8 (Figs. 8, 9).
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Figure 8. Distribution of labeled terminals and cell bodies after a WGA-HRP injection into TEav (Case: 4). The striped regions in the unfolded map (in pmts and ots) indicate the distribution of labeled terminals without labeled cell bodies. The labeled regions indicated by the boxes in coronal sections 84 and 32 are shown in the dark-field photomicrographs in Figure 7, C and D, respectively. In STS, the distribution of labeling was limited to the rostral part of the lower bank. The brain regions beyond the vertical lines in the unfolded map were not examined. Other conventions are as in Figure 3.
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Figure 9. Distribution of labeled terminals and cell bodies after a WGA-HRP injection into TEav (case: 5). The small filled regions in the unfolded map (in pmts) indicate the distribution of labeled cell bodies without labeled terminals. The striped regions in the unfolded map (in pmts and ots) indicate the distribution of labeled terminals without labeled cell bodies. The brain regions posterior to the vertical line in the unfolded map were not examined.
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Figure 10. Distribution of anterogradely labeled terminals after a small PHA-L injection into TEav (case: 6). The brain regions caudal to the area circumscribed by broken lines in the lateral view of the brain were not examined. Other conventions are as in Figures 3 and 5.
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Figure 11. Distribution of anterogradely labeled terminals after a small PHA-L injection into TEav (case: 7). The brain regions caudal to the area circumscribed by broken lines in the lateral view of the brain were not examined. All other conventions are the same as in Figures 3 and 5.
In both WGA-HRP and PHA-L cases, the labeled terminals in STS were distributed in all the cortical layers (Figs. 7C, 8, section 84; Fig. 8, section 78; Fig. 9, section 54; Fig. 10, section 234; Figs. 10, 12, section 263; Fig. 11, sections 346, 357, and 382) with the highest density always in layer 2 and the upper part of layer 3 (Fig. 12). In some cases, the terminals appeared in the deep layers (5-6) and gradually moved to the upper layers (1-3) (e.g., sections 193, 202, and 214 in Fig. 10). This movement seems to be caused by the cutting of sections oblique to the axis of cortical columns (see Materials and Methods). The labeled terminals in layer 4 were as dense as those in layer 5 and the lower part of layer 3 (Fig. 12). The labeled terminals in layer 1 were sparser than those in layer 2 and the upper part of layer 3. The cell bodies retrogradely labeled in the WGA-HRP cases were equally distributed in layers 2-3 and 5-6 (Figs. 7C, 8, section 84) but also found more in layers 2-3 in some sections. The predominant distribution of labeled cell bodies in layers 2-3 was observed in the caudal and rostral edges of labeled zones. A few labeled cell bodies were occasionally found in layer 4 in some sections.
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Figure 12. High magnification camera lucida drawing of a patchy region in the lower bank of the rostral STS showing the laminar distribution of PHA-L-labeled terminals in case 6. The position of the patch in section 263 is indicated by a box in the inset on the right. Labeled terminals were distributed in all the cortical layers, but they were found more predominantly in layer 2 and the upper part of layer 3.
Clusters of labeling were also found in TEO and the TEpv. The most prominent clusters were located in the lateral bank and lateral lip of the OTS in all five cases (Figs. 8-11), and less prominent clusters were located at more lateral regions on the ventrolateral surface in most cases (Figs. 8, 9, 11). The labeling was also found in the PMTS in three WGA-HRP cases (Figs. 8, 9), whereas this sulcus was not included in the section cutting in the two PHA-L cases (Figs. 10, 11). Some of the clusters in the occipitotemporal sulcus and posterior middle temporal sulcus contained only labeled terminals (Figs. 8, 9, hatched regions) or cell bodies (Fig. 9, small filled regions in pmts). The clusters in the lateral bank and lip of the occipitotemporal sulcus were continuous with the distribution of labeling surrounding the injection within TEav in most cases (Figs. 8, 10, 11). The distribution of labeling surrounding the injection sites also expanded to the perirhinal cortex in all five cases. We have described these projections from TEav to the perirhinal cortex in a previous paper (Saleem and Tanaka, 1996
Labeled terminals were found in both layers 1-3 and 5-6 in most of these posterior clusters (Figs. 7D, 8, section 32). Labeled terminals were also observed in layer 4 in some sections (Fig. 7D, section 33), but the concentrations in layer 4 were always lower than in layer 5 and the lower part of layer 3. Cell bodies retrogradely labeled in the WGA-HRP cases were found in both layers 2-3 and 5-6, with denser distribution in layers 2-3 (Fig. 7D, section 33), or largely confined to layers 2-3 (Fig. 7D, section 32).
TEav/36 border case and area 36 case
The injection sites in the above-described TEav cases were always located at the medial lip of the anterior middle temporal sulcus. TEav extends to the ventral surface medial to these injection sites (Saleem and Tanaka, 1996
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Figure 13. Distribution of labeled terminals and cell bodies after a WGA-HRP injection into the border between TEav and area 36 of the perirhinal cortex (case: 9). The striped regions in the unfolded map (ots) indicate the distribution of labeled terminals without labeled cell bodies. The brain regions anterior to the vertical line were not examined. Other conventions are the same as in Figure 3.
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Figure 14. Distribution of labeled terminals and cell bodies after a WGA-HRP injection into the caudal part of area 36 of the perirhinal cortex (case: 10). For other conventions see Figure 3.
In the TEav/36 border injection case, the distribution of labeling was confined to the lower bank of the rostral STS (Fig. 13), as in the TEav cases. The distribution of labeling was split into several small clusters with an overall rostrocaudal extent similar to that of the large clusters in case 4 (Fig. 8) and case 8 with TEav injections, except that there was one cluster in TG in the TEav/36 case. In the area 36 case there were again several clusters of labeling in the lower bank of the rostral STS as in the TEav and TEav/36 border cases, but there was also a distinctive cluster of labeling in the upper bank of the rostral end of STS (Fig. 14, section 99). This part of STS did not contain labeling in both TEad and TEav cases.
In the TEav/36 border case, the labeled terminals were distributed in all cortical layers, and the labeled cell bodies were distributed in both layers 2-3 and 5-6 in the lower bank of the rostral STS (Fig. 13, section 115). In the area 36 case, the labeled terminals were mostly confined to layers 1-3 and the labeled cell bodies to layers 2-3 in the lower bank of the rostral STS (Fig. 14, section 88). However, the labeled terminals were distributed in all cortical layers and the labeled cell bodies in both layers 2-3 and 5-6 of the upper bank of the rostral end of STS (Fig. 14, section 99).
STP case
We found that TEad was reciprocally connected with the upper bank of the rostral STS (STP), whereas TEav did not have connections with this STS region. To confirm these findings, we placed a WGA-HRP injection in the upper bank of the rostral STS in one case (Fig. 15, case 11). The injection was actually located at the upper lip of STS at the rostrocaudal level corresponding to TEad, and it covered parts of the superior temporal gyrus as well as the upper bank of STS. It covered all cortical layers. In addition to the dense distribution of labeling in STS and the superior temporal gyrus, there were discrete clusters of labeling in TEad (Fig. 15, section 108). There was also a sparse cluster of labeling within the medial bank of the RS, which corresponds to the lateral part of the entorhinal cortex (area 28). The labeling slightly invaded area 35 of the perirhinal cortex at the rostral end.
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Figure 15. Distribution of labeled terminals and cell bodies after a WGA-HRP injection into the upper bank of rostral STS in the superior temporal polysensory area (STP) (case: 11). Labeling was found in TEad but not in TEav. Other conventions are as in Figure 3.
In the clusters found in TEad and the rhinal sulcus, the labeled terminals were distributed in all cortical layers, and the labeled cell bodies were distributed in both layers 2-3 and 5-6 or confined to layers 2-3. Labeled terminals and cell bodies of various densities were found in the parahippocampal gyrus, insula, cingulate, and CA1 region of the hippocampus, which are not shown in Figure 15. No labeled terminals or cell bodies were found in TEav, more posterior inferotemporal regions (TEpd, TEpv, TEO), or area 36 of the perirhinal cortex.
DISCUSSION
Connections of TEad and TEav with rostral STS
The present study reveals a dichotomy in the connections of TEad and TEav with the rostral STS. TEad connects with the upper bank of rostral STS, whereas TEav connects with the lower bank and fundus of rostral STS. The known differences in TEad and TEav connections are illustrated in Figure 16.
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Figure 16. Top, Summary diagram of the projections from TEad, TEav, and area 36 of the perirhinal cortex to different regions in STS. The heavy solid lines denote dense projections, and thin solid lines denote moderate to sparse projections. Arrowhead at the rostral end of the flattened map indicates the border between TG and TEad. Bottom, Connections of TEad and TEav with STS, the posterior inferotemporal cortex, and the medial temporal lobe structures based on the present and previous studies (Yukie et al., 1990
Our results challenge the classical view that the lower bank of rostral STS is connected with TE, whereas the upper bank of rostral STS is connected with the parietal, prefrontal, and superior temporal regions (Seltzer and Pandya, 1978
The present study also shows that TEad and TEav projections are distributed to all cortical layers in most parts of the terminal fields in the rostral STS. Cells projecting back to TEad and TEav were located in layers 2-3 and 5-6 in the rostral STS. These laminar patterns of labeled terminals and cell bodies are similar to those of the "lateral type" projections in sensory pathways (Rockland and Pandya, 1979
Connections of TEad and TEav with posterior areas
The present study found that TEad is heavily connected with the lower bank of the rostrocaudally middle part of STS, whereas TEav is heavily connected with the lateral lip and lateral bank of the occipitotemporal sulcus, which correspond to TEpv or the ventral part of TEO. The laminar pattern of terminal distribution of the projections from TEad and TEav to these posterior regions are consistent with those of the "feedback type," and the laminar patterns of the cells projecting from the posterior regions to TEad and TEav are consistent with those of the "feedforward type," suggesting that TEad and TEav are higher than the posterior regions in the connectional hierarchy (Felleman and Van Essen, 1991
These findings are consistent with the results of Martin-Elkins and Horel (1992)
Functional significance
The upper bank of the rostral STS is known to be polymodal because it receives converging projections from the parietal, prefrontal, and superior temporal regions (Seltzer and Pandya, 1978
A possible function of the projection from the anterior STP to TEad is to provide the spatial context of objects to the analysis of object images in TEad via anterior STP afferents from parietal and prefrontal regions. The responses to optical flow support the idea that the anterior STP is involved in processing of spatial information. TEad may also receive spatial information from the parahippocampal gyrus: there are moderate to strong projections from the parahippocampal gyrus to TEad but not to TEav (Webster et al., 1991
The afferents to the lower bank of the rostral STS are less convergent than those to the upper bank. More caudal parts of the lower bank of STS (Seltzer and Pandya, 1989b
We have suggested previously that TEav is more involved in recognition memory than TEad because we found that TEav more strongly projected to the perirhinal cortex than did TEad (Saleem and Tanaka, 1996
FOOTNOTES Received Feb. 23, 2000; revised April 10, 2000; accepted April 11, 2000.
This work was supported by the Riken Brain Science Institute. We thank A. H. Asiya Begum for surgical and histological assistance.
Correspondence should be addressed to Dr. K. S. Saleem, Laboratory for Neural Architecture, Riken Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan. E-mail: saleem{at}postman.riken.go.jp.
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