Subdivisions and connections of inferior temporal cortex in owl monkeys

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Abstract
Patterns of cortical connections and differences in architectonic appearance were used to subdivide inferior temporal cortex of owl monkeys into four main regions. These regions were named by location: ITc (the caudal subdivision of inferior temporal cortex), ITR (the rostral subdivision of inferior temporal cortex), ITp (the polar subdivision of inferior temporal cortex), and ITM (the medial subdivision of inferior temporal cortex). Two of these regions may contain further subdivisions–ITC, separate dorsal and ventral areas, and ITM medial and lateral areas. The most caudal subdivision, ITC, was defined in an earlier report (Weller and Kaas: J. Comp. Neurol. 234:35–59, '85) as the projection zone of the dorsolateral visual area (DL). ITC occupies roughly the caudal half of the architectonic zone temporal area E (TE) (after von Bonin and Bailey: The Neocortex of Macaca mulatta. Urbana: University of Illinois Press, '47). TE is characterized by a dense, broad layer IV of granule cells and a dark inner band of myelination. Injections of 3H‐proline in ITC demonstrated major projections to a more rostral division of the temporal lobe, ITR. Other projections were to the frontal eye field (FEF), a more ventral region of frontal cortex (FV), and a medial division of inferior temporal cortex, ITM, on the ventral surface of the temporal lobe. Feedback projections of ITC were to DL and adjoining temporal‐parietal cortex (TP), while interhemispheric projections were to ITC and ITR. Connections between dorsal and ventral ITC, together with earlier evidence for two projection zones of DL in ITC (Weller and Kaas: ibid., '85), suggest that dorsal and ventral sectors of ITC are separate visual areas. The rostral division of inferior temporal cortex, ITR, was defined as the projection zone of ITC. ITR occupied the rostral half of the architectonic region TE. Slight differences in cortical architecture between ITC and ITR were noted, but an architectonic border between the two fields could not be reliably distinguished. Injections in ITR demonstrated projections to the rostral pole of temporal cortex, ITP, feedback projections to ITC, and inputs to FEF, FV, dorsomedial frontal cortex, and the rostroventral superior temporal gyrus. Interhemispheric projections were to ITR and ITP. The projections of ITR to the rostral pole defined ITP. ITP has broad, less distinct layers of cortex and appears to correspond to temporal area G (TG) of von Bonin and Bailey (ibid., '47). The only known input to ITP is from ITR, and its projections have not yet been determined. The fourth major division of inferior temporal cortex, ITM, is medial to ITC and ITR on the ventral surface of the temporal lobe. Most of area ITM is coextensive with area TF of von Bonin and Bailey (ibid., '47). Area TF has a reduced layer IV of granule cells and a thin and pale inner band of myelination. A small medial portion of ITM, just caudal to entorhinal cortex, was identified as area TH of von Bonin and Bailey (ibid., '47). Area TH is characterized by a fusion of granular and supragranular layers. ITM receives inputs from the dorsointer‐mediate area, DI, and the superior temporal area, ST (Weller et al.: J. Comp. Neurol. 228231‐104, '84). DI projects most densely to lateral ITM, while ST projects most densely to medial ITM. ITc and probably also ITR project weakly to lateral ITM. It is not certain that the differences in connections between lateral and medial ITM correspond to the architectonic distinction between TF and TH, but the results do suggest the existance of two fields within ITM. The major cortical input to ITC cortex is compatible with the proposed role of IT in object recognition (for review see Ungerleider and Mishkin: “Two cortical visual systems.” In D.J. Ingle, J.W. Mansfield, and M.A. Goodale (eds):Advances in the Analysis of Visual Behavior. Cambridge: MIT Press, '82). Thus, the major visual projection to ITc in owl monkeys originates from DL. This input, in turn, depends on relays through V‐11, V‐I, and the parvocellular (X‐like) geniculate laminae. ITc relays to ITR, and ITR provides a major input to ITp. ITc also relates to visuomotor centers in the frontal lobe, while ITR has more widely distributed frontal lobe connections suggesting a broader role in visual behavior. Although lateral ITM receives input similar to that of ITc, medial ITM receives input from ST, which may receive Y‐like visual input via a relay through cells in magnocellular genic‐ulate layers to V‐I and then the middle temporal visual area, MT. Thus, in contrast to other divisions of IT cortex, medial ITM is associated with a subsystem that is also directed to posterior parietal cortex and is generally thought to be important in visual attention (e.g., Ungerleider and Mishkin, ibid., '82).