Qualitative and quantitative features of axons projecting from caudal to rostral inferior temporal cortex of squirrel monkeys.

On the basis of cortical and subcortical connections and architectonics, inferior temporal (IT) cortex of squirrel monkeys consists of a caudal region, ITC, with dorsal (ITCd) and ventral (ITCv) subdivisions; a rostral region, ITR; and possibly a third region intermediate to ITC and ITR, ITI (Weller & Steele, 1992; Steele & Weller, 1993). The present study qualitatively and quantitatively examined the terminal arborizations of 26 axons in ITR and ITI labeled by injections of biocytin or, in one case, horseradish peroxidase, in ITCv. The majority of axons gave rise to a single terminal arbor, with a small number branching into two overlapping or nearby arbors. Presumptive terminal specializations consisted of rounded, bead-like swellings, most often located en passant. All axons terminated in layer 4 of cortex, and most had additional terminations in layers 3 and 5. The total extent of each axon's terminal arbor was 125-750 microns dorsoventrally (mean = 360.6 microns) and 150-725 microns anteroposteriorly (mean = 328.1 microns; all values uncorrected for shrinkage). In most axons, especially those with larger terminal fields, boutons were not uniformly distributed, but formed 2-4 clumps (mean = 2.2), with a mean width of 149 microns, separated by narrower regions of fewer boutons. Based on a cluster analysis of characteristics of the 26 axons, axons projecting from caudal (ITCv) to rostral (ITR or ITI) IT cortex of squirrel monkeys comprised three groups that we called Type I, Type II, and Type III. Type I axons, the smallest in area extent of terminal arbor, terminated predominantly in dorsal ITR. Type III axons, largest in areal extent, and Type II axons, intermediate in areal extent, terminated in ventral ITR and throughout ITI. The three classes of axons may correspond to different types of visual information entering rostral IT cortex. The clumping of boutons suggests that individual axons terminate in limited patches within their terminal fields.

Subcortical connections of subdivisions of inferior temporal cortex in squirrel monkeys.

On the basis of cortical connections and architectonics, inferior temporal (IT) cortex of squirrel monkeys consists of a caudal, prestriate-recipient region, ITC; a rostral region, ITR; and possibly an intermediate region along the border of ITC and ITR, "ITI" (Weller & Steele, 1992). ITC contains dorsal (ITCd) and ventral (ITCV) areas. The subcortical connections of these subdivisions of IT cortex were determined in the present study from the results of cortical injections of wheat-germ agglutinin conjugated to horseradish peroxidase, [3H]-amino acids and fast blue. ITC and ITR receive afferents from the locus coeruleus, dorsal raphe, nucleus annularis, central superior nucleus, pontine reticular formation, lateral hypothalamus, paracentral nucleus, and central medial nucleus; send efferents to the superior colliculus, reticular nucleus, and striatum; and have both afferent and efferent connections with the pretectum, pulvinar, claustrum, amygdala, and basal nucleus of Meynert. ITC and ITR have different patterns of connections with a number of subcortical structures, including the pulvinar and amygdala. Injections in ITC strongly label multiple nuclei of the inferior pulvinar and the medial division of the lateral pulvinar (PLM), and moderately label the medial pulvinar (PM), whereas injections in ITR strongly label PM and moderately label PLM. Injections in ITC label sparse projections to the lateral nucleus of the amygdala, in contrast to injections in ITR that label strong projections to the lateral and basal nuclei of the amygdala. Injections in "ITI" produce a pattern of subcortical label that has some features of that observed from injections in ITC and that observed from injections in ITR. Although most of the connections of ITCd and ITCv appear similar, only injections involving ITCd label the middle nucleus of the inferior pulvinar (PIM). Comparison of the subcortical connections of subdivisions of IT cortex in squirrel monkeys and what is presently known of the subcortical connections of subdivisions of IT cortex in macaque monkeys supports the previous suggestion that ITC of squirrel monkeys may be comparable to area TEO of macaques, ITI may be comparable to posterior area TE, and ITR may be comparable to anterior area TE (Weller & Steele, 1992).

Cortical connections of subdivisions of inferior temporal cortex in squirrel monkeys.

Patterns of cortical connections and architectonics were used to determine subdivisions of inferior temporal (IT) cortex of squirrel monkeys. Single or multiple injections of the tracers wheat germ agglutinin-horseradish peroxidase, Fast Blue, Diamidino Yellow, Fluoro-Gold, and 3H-amino acids were placed into IT cortex. Most injections were placed in caudal IT cortex in the region previously shown to receive input from the caudal subdivision of the Dorsolateral Area, DLC; additional injections were placed in more rostral IT cortex. The results indicate the presence of two major regions: a caudal region, ITC, and a rostral region, ITR. An intermediate region of cortex along the ITC-ITR border that displays some connections of ITC and some connections of ITR may be another area. ITC contains a more myelinated dorsal area, ITCd, and a larger ventral area, ITCv. Both ITCd and ITCv receive a major projection from DLC; additional input from DLR, MT, and VII; and send strong projections to ITR, the lateral bank of the superior temporal sulcus, and dorsolateral prefrontal cortex. Only ITCd has strong connections with DLR and cortex in the depths of the superior temporal sulcus, and only ITCv has connections with lateral orbital cortex. The overall pattern of connections between ITC and DLC suggests that ITC has a crude topographic organization, with dorsal cortex representing the lower field and ventral cortex representing the upper field. ITR differs from ITC by receiving little if any input from DLC; projecting to inferior temporal polar cortex, the rostral Sylvian fissure, and medial orbital cortex; and having a less distinct layer IV. Comparison of subdivisions of inferior temporal cortex defined in the present study in squirrel monkeys and those reported in other primates suggests that ITC of squirrel monkeys may correspond to area TEO of macaque monkeys.

Cortical connections of the caudal subdivision of the dorsolateral area (V4) in monkeys.

Evidence suggests that all primates have rostral and caudal subdivisions in the region of visual cortex identified as the dorsolateral area (DL) or V4. However, the connections of DL/V4 have not been examined in terms of these subdivisions. To determine the cortical connections of the caudal subdivision of DL (DLC) in squirrel monkeys, injections of the neuroanatomical tracers wheat germ agglutinin conjugated to horseradish peroxidase, Diamidino Yellow, and Fluoro-Gold were made in cortex rostral to V II. To aid in delineating the borders of DLC, cortex was also evaluated architectonically. Based on similar patterns of connections, DLC extends from dorsolateral to ventrolateral cortex. DLC receives strong, feedforward input from V II and projects in a feedforward fashion to the rostral subdivision of DL (DLR) and caudal inferior temporal (IT) cortex, including a separate location in the inferior temporal sulcus. DLC has weaker connections with V I, the middle temporal area (MT), cortex rostral to MT in the location of the fundal superior temporal area (FST), cortex dorsal to DLC, ventral cortex rostral to V II, and cortex in the frontal lobe, lateral to the inferior arcuate sulcus. Only lateral DLC has connections with V I, and only dorsolateral DLC has connections with cortex dorsal to DLC. The topographic organization of DLC was inferred from its connections with V II. Thus, dorsolateral DLC represents the lower field, lateral DLC represents central vision, and ventrolateral DLC represents the upper field. Limited observations were made on DLR. Confirming earlier observations (Cusick and Kaas: Visual Neurosci. 1:211, 1988), DLR is paler than DLC myeloarchitectonically. DLR receives only sparse feedforward input from V II, but stronger input from DLC. DLR has strong connections with cortex just rostral to dorsal V II, ventral posterior parietal cortex in the sylvian fissure, MT, the medial superior temporal area, FST, and the inferior temporal sulcus. DLR also shares connections with IT cortex. Thus, while both DLC and DLR are involved in the pathway relaying visual information to IT cortex, an area specialized for object vision, DLR also projects densely to areas such as MT involved in the pathway relaying to posterior parietal cortex, a region specialized for spatial localization and motion perception.

Cortical connections of dorsal cortex rostral to V II in squirrel monkeys.

A region of dorsal cortex along the rostral border of V II has been described as comprising a visual area or areas separate from more lateral cortex in both New and Old World primates. To evaluate these possibilities in squirrel monkeys, we studied patterns of cortical connections by injecting Fast Blue, Fluoro-Gold, horseradish peroxidase, and wheat germ agglutinin conjugated to horseradish peroxidase into the dorsal region and related results to distinctions in myeloarchitecture. Our major conclusions are as follows. 1) The dorsal region (D) has distinctly different connections from the area found laterally, the caudal subdivision of the dorsolateral area (DLC). These include major connections with the rostral subdivision of the dorsolateral area (DLR), ventral posterior parietal cortex in the Sylvian fissure, the middle temporal area (MT), the medial superior temporal area (MST), ventral cortex just rostral to V II, and cortex in the inferior temporal sulcus. Weaker connections are with V I, V II, DLC, the fundal superior temporal area (FST), and the frontal lobe. In contrast, DLC has strong connections with V II and inferior temporal (IT) cortex, weaker connections with DLR, and lacks connections with ventral posterior parietal cortex (Steele et al: J Comp Neurol 306:495-520, 1991). 2) Caudal and rostral aspects of dorsal cortex differ in the magnitude of connections with V I, V II, DLR, and FST. These differences are consistent with the previous proposal that at least two visual areas, caudal and rostral, occupy the dorsal region in squirrel monkeys (Krubitzer and Kaas: Visual Neurosci 5:165, 1990), but they could also reflect regional differences in the connections of a single visual area. 3) The dorsal region is more densely myelinated than surrounding cortex; however, rostral aspects of dorsal cortex are less myelinated than caudal aspects, again suggesting the existence of at least two areas. 4) The distinctiveness of connections between dorsal cortex and rostral as compared to caudal dorsolateral cortex provides further evidence for dividing the region of DL into two visual areas, DLC and DLR (Cusick and Kaas: Visual Neurosci 1:211, 1988; Steele et al: J Comp Neurol 306:495-520, 1991).