Distinct Feedforward and Intrinsic Neurons in Posterior Inferotemporal Cortex Revealed by in Vivo Connection Imaging

We investigated circuits for object recognition in macaque anterior (TE) and posterior inferotemporal cortex (TEO), using a two-step method with in vivo anatomical imaging. In step 1, red fluorescent tracer was injected into TE to reveal and Pre-target patches of feedforward neurons in TEO. In step 2, these were visualized on the cortical surface in vivo, and injected with green fluorescent tracer. Histological processing revealed that patches >500 μm from the injection site in TEO consisted of intermingled green TEO intrinsically projecting neurons and red TEO-to-TE neurons, with only few double-labeled neurons. In contrast, patches near the injection site in TEO contained many double-labeled neurons. Two parallel, spatially intermingled circuits are suggested: (1) TEO neurons having very local intrinsic collaterals and projection to TE (2) TEO neurons projecting more widely in the intrinsic network, but not to TE. These parallel systems might be specialized for, respectively, fast vs. highly processed signals.

[1]  Mark C. W. van Rossum,et al.  Adaptive Integration in the Visual Cortex by Depressing Recurrent Cortical Circuits , 2008, Neural Computation.

[2]  A. L. Humphrey,et al.  Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis) , 1982, The Journal of comparative neurology.

[3]  J. Tanji,et al.  Origins of multisynaptic projections from the basal ganglia to rostrocaudally distinct sectors of the dorsal premotor area in macaques , 2011, The European journal of neuroscience.

[4]  K. Tanaka,et al.  Divergent Projections from the Anterior Inferotemporal Area TE to the Perirhinal and Entorhinal Cortices in the Macaque Monkey , 1996, The Journal of Neuroscience.

[5]  Leslie G. Ungerleider,et al.  Visual topography of area TEO in the macaque , 1991, The Journal of comparative neurology.

[6]  Keiji Tanaka,et al.  Inferotemporal cortex and object vision. , 1996, Annual review of neuroscience.

[7]  H. Komatsu,et al.  Reciprocal connectivity of identified color-processing modules in the monkey inferior temporal cortex. , 2011, Cerebral cortex.

[8]  L. Haberly,et al.  New Features of Connectivity in Piriform Cortex Visualized by Intracellular Injection of Pyramidal Cells Suggest that “Primary” Olfactory Cortex Functions Like “Association” Cortex in Other Sensory Systems , 2000, The Journal of Neuroscience.

[9]  L C Katz,et al.  Local circuitry of identified projection neurons in cat visual cortex brain slices , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  E. Rolls,et al.  Speed of feedforward and recurrent processing in multilayer networks of integrate-and-fire neurons , 2001, Network.

[11]  I Fujita,et al.  Intrinsic connections in the macaque inferior temporal cortex , 1996, The Journal of comparative neurology.

[12]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

[13]  D J Felleman,et al.  Modular Organization of Occipito-Temporal Pathways: Cortical Connections between Visual Area 4 and Visual Area 2 and Posterior Inferotemporal Ventral Area in Macaque Monkeys , 1997, The Journal of Neuroscience.

[14]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[15]  Lawrence C. Sincich,et al.  The circuitry of V1 and V2: integration of color, form, and motion. , 2005, Annual review of neuroscience.

[16]  Emery N. Brown,et al.  Functional Biases in Visual Cortex Neurons with Identified Projections to Higher Cortical Targets , 2012, Current Biology.

[17]  Keiji Tanaka,et al.  Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. , 1994, Journal of neurophysiology.

[18]  Scott L. Brincat,et al.  Dynamic Shape Synthesis in Posterior Inferotemporal Cortex , 2006, Neuron.

[19]  F. Fujiyama,et al.  Exclusive and common targets of neostriatofugal projections of rat striosome neurons: a single neuron‐tracing study using a viral vector , 2011, The European journal of neuroscience.

[20]  Marta Kutas,et al.  Neurophysiological Evidence for the Time Course of Activation of Global Shape, Part, and Local Contour Representations during Visual Object Categorization and Memory , 2007, Journal of Cognitive Neuroscience.

[21]  E M Callaway,et al.  Layer-Specific Input to Distinct Cell Types in Layer 6 of Monkey Primary Visual Cortex , 2001, The Journal of Neuroscience.

[22]  Manabu Tanifuji,et al.  Cortical Connections to Area TE in Monkey: Hybrid Modular and Distributed Organization , 2009, Cerebral cortex.

[23]  K. Rockland,et al.  Axon collaterals of meynert cells diverge over large portions of area V1 in the macaque monkey , 2001, The Journal of comparative neurology.

[24]  Thomas K. Berger,et al.  A synaptic organizing principle for cortical neuronal groups , 2011, Proceedings of the National Academy of Sciences.

[25]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[26]  Doris Y. Tsao,et al.  Patches with Links: A Unified System for Processing Faces in the Macaque Temporal Lobe , 2008, Science.

[27]  J. B. Levitt,et al.  Patterns of intrinsic and associational circuitry in monkey prefrontal cortex , 1996, The Journal of comparative neurology.

[28]  Farran Briggs,et al.  Laminar patterns of local excitatory input to layer 5 neurons in macaque primary visual cortex. , 2005, Cerebral cortex.

[29]  P. Strick,et al.  An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. , 2003, Journal of neurophysiology.

[30]  R. Beauchamp VISION, MEMORY, AND THE TEMPORAL LOBE , 1991 .

[31]  Leslie G. Ungerleider,et al.  Subcortical connections of inferior temporal areas TE and TEO in macaque monkeys , 1993, The Journal of comparative neurology.

[32]  W. Suzuki,et al.  Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  S. Zeki Are areas TEO and PIT of monkey visual cortex wholly distinct from the fourth visual complex (V4 complex) ? , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.