Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Perception of Objects Hierarchically in Occipitotemporal Cortices


Science 12 July 2013: Vol. 341 no. 6142 pp. 191-195

Microcircuits for Hierarchical Elaboration of Object Coding Across Primate Temporal Areas

Toshiyuki Hirabayashi, Daigo Takeuchi, Keita Tamura, Yasushi Miyashita

Department of Physiology, The University of Tokyo School of Medicine, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.

Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Kawaguchi, Saitama 332-0012, Japan.

Department of Brain Sciences, Center for Novel Science Initiatives, National Institutes of Natural Sciences, Toranomon 4-3-13, Minato-ku, Tokyo 105-0001, Japan.


In primates, neuronal representations of objects are processed hierarchically in occipitotemporal cortices. A “novel” feature of objects is thought to emerge and become prevalent at a cortical area because of processing in this area. We tested the possibility that a feature representation prevalent in a given area emerges in the microcircuit of a hierarchically prior area as a small number of prototypes and then becomes prevalent in the subsequent area. We recorded multiple single units in each of hierarchically sequential areas TE and 36 of macaque temporal cortex and found the predicted convergent microcircuit for object-object association in area TE. Associative codes were then built up over time in the microcircuit of area 36. These results suggest a computational principle underlying sequentially elaborated object representations.

Neuronal representations of objects are processed hierarchically in the primate occipitotemporal lobe. Representations of a “novel” feature that constitutes a given object are thought to emerge and become prevalent in one of the areas in the cortical hierarchy. Although this sudden emergence and prevalence of novel feature representations have been established for the transformation from a lateral geniculate nucleus to V1 in the visual processing pathway, it is not known whether the same principle holds for the corticocortical hierarchy.

Previous studies have demonstrated that single neurons representing associations between two object images (pair-coding neurons) become prevalent in area 36 of the perirhinal cortex, whereas the pair-coding neurons only constitute a small minority in area TE, a hierarchically prior cortical area. We looked for microcircuits that generated pair-coding neurons in areas TE and 36 by simultaneously recording from multiple single neurons in each of these areas while monkeys performed a pair-association memory task. Conventional cross-correlation analyses were conducted to detect functional connectivity between recorded neurons.

Previous studies have attempted to uncover the functional hierarchy of cortical processing by showing the areal differences in the response properties of single units and presumed that novel feature representations emerge and become prevalent within a single cortical area. In the present study, we instead demonstrated the areal differences in the computational principles by detecting the functional microcircuits from different cortical areas and suggest that the prevalence of elaborated object representations in a cortical area can be attained by emergence of the representations through the specific microcircuit computations in a prior area and subsequent building up over time in the microcircuit of the next area.

The microcircuits for associative object representations found in the present study might act in parallel with other channels, including feedforward functional convergence from area TE, top-down feedback from the prefrontal and/or medial temporal cortices, thalamic contributions, and across-laminar interactions. Elucidating the entire view of across-areal elaboration of object representations will be an important issue for future studies to manifest the computational principles of the hierarchical brain.

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