Computational principles of microcircuits for visual object processing in the macaque temporal cortex

Understanding the principles of neuronal computation that underlie our cognitive abilities is a fundamental goal of neuroscience. Microcircuits are thought to be computational units embedded in a brain-wide neuronal network. Recent progress in experimental and analytical techniques has enabled the exploration of information flow in operating microcircuits of behaving monkeys. Accumulating evidence demonstrates that crucial transformations of neuronal codes for the representation and memory retrieval of visual objects occur in cortical microcircuits. Particularly, microcircuit comparisons across cortical areas provide novel principles for object processing, in which precursor codes for object features are constructed in a lower-order area before prevalence in a higher-order area. We review recent findings on microcircuit operations in macaque temporal cortex that enable object processing, and discuss future research directions.

[1]  Mingzhou Ding,et al.  Analyzing multiple spike trains with nonparametric granger causality , 2009, Journal of Computational Neuroscience.

[2]  Nicolas Brunel,et al.  Dynamics and plasticity of stimulus-selective persistent activity in cortical network models. , 2003, Cerebral cortex.

[3]  Emery N. Brown,et al.  A Granger Causality Measure for Point Process Models of Ensemble Neural Spiking Activity , 2011, PLoS Comput. Biol..

[4]  Y. Miyashita,et al.  Microcircuits for Hierarchical Elaboration of Object Coding Across Primate Temporal Areas , 2013, Science.

[5]  Ifije E. Ohiorhenuan,et al.  Sparse coding and high-order correlations in fine-scale cortical networks , 2010, Nature.

[6]  Y. Saalmann,et al.  The Pulvinar Regulates Information Transmission Between Cortical Areas Based on Attention Demands , 2012, Science.

[7]  Charles E Connor,et al.  Underlying principles of visual shape selectivity in posterior inferotemporal cortex , 2004, Nature Neuroscience.

[8]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

[9]  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.

[10]  György Buzsáki,et al.  Neural Syntax: Cell Assemblies, Synapsembles, and Readers , 2010, Neuron.

[11]  Valentin Dragoi,et al.  Adaptation-induced synchronization in laminar cortical circuits , 2011, Proceedings of the National Academy of Sciences.

[12]  J. Alonso,et al.  Functional connectivity between simple cells and complex cells in cat striate cortex , 1998, Nature Neuroscience.

[13]  G. P. Moore,et al.  Statistical signs of synaptic interaction in neurons. , 1970, Biophysical journal.

[14]  Keiji Tanaka,et al.  Effects of shape-discrimination training on the selectivity of inferotemporal cells in adult monkeys. , 1998, Journal of neurophysiology.

[15]  Y. Sakurai.  How do cell assemblies encode information in the brain? , 1999, Neuroscience & Biobehavioral Reviews.

[16]  T. Mexia,et al.  Author ' s personal copy , 2009 .

[17]  Karl J. Friston,et al.  Canonical Microcircuits for Predictive Coding , 2012, Neuron.

[18]  Yasushi Miyashita,et al.  Dynamically Modulated Spike Correlation in Monkey Inferior Temporal Cortex Depending on the Feature Configuration within a Whole Object , 2005, The Journal of Neuroscience.

[19]  R. Freeman,et al.  Stereoscopic depth processing in the visual cortex: a coarse-to-fine mechanism , 2003, Nature Neuroscience.

[20]  Katarzyna J. Blinowska,et al.  A new method of the description of the information flow in the brain structures , 1991, Biological Cybernetics.

[21]  Tomoki Fukai,et al.  Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements , 2009, Nature Neuroscience.

[22]  Robert E. Hampson,et al.  Columnar Processing in Primate pFC: Evidence for Executive Control Microcircuits , 2012, Journal of Cognitive Neuroscience.

[23]  Peter König,et al.  On the directionality of cortical interactions studied by structural analysis of electrophysiological recordings , 1999, Biological Cybernetics.

[24]  Todd P. Coleman,et al.  Estimating the directed information to infer causal relationships in ensemble neural spike train recordings , 2010, Journal of Computational Neuroscience.

[25]  Asohan Amarasingham,et al.  Internally Generated Cell Assembly Sequences in the Rat Hippocampus , 2008, Science.

[26]  C. Gilbert,et al.  Topography of contextual modulations mediated by short-range interactions in primary visual cortex , 1999, Nature.

[27]  David L. Sheinberg,et al.  Effects of Long-Term Visual Experience on Responses of Distinct Classes of Single Units in Inferior Temporal Cortex , 2012, Neuron.

[28]  Yasushi Miyashita,et al.  Forward Processing of Long-Term Associative Memory in Monkey Inferotemporal Cortex , 2003, The Journal of Neuroscience.

[29]  Y. Miyashita,et al.  Neural organization for the long-term memory of paired associates , 1991, Nature.

[30]  Yasushi Miyashita,et al.  Triphasic Dynamics of Stimulus-Dependent Information Flow between Single Neurons in Macaque Inferior Temporal Cortex , 2010, The Journal of Neuroscience.

[31]  C. Schroeder,et al.  Neuronal Mechanisms of Cortical Alpha Oscillations in Awake-Behaving Macaques , 2008, The Journal of Neuroscience.

[32]  T. Albright.  On the Perception of Probable Things: Neural Substrates of Associative Memory, Imagery, and Perception , 2012, Neuron.

[33]  C. Connor,et al.  Neural representations for object perception: structure, category, and adaptive coding. , 2011, Annual review of neuroscience.

[34]  Melanie R. Bernard,et al.  Deconstruction of Spatial Integrity in Visual Stimulus Detected by Modulation of Synchronized Activity in Cat Visual Cortex , 2008, The Journal of Neuroscience.

[35]  Alexander Maier,et al.  Infragranular Sources of Sustained Local Field Potential Responses in Macaque Primary Visual Cortex , 2011, The Journal of Neuroscience.

[36]  A. Treves,et al.  Converging Neuronal Activity in Inferior Temporal Cortex during the Classification of Morphed Stimuli , 2008, Cerebral cortex.

[37]  T. Hafting,et al.  Frequency of gamma oscillations routes flow of information in the hippocampus , 2009, Nature.

[38]  Sonja Grün,et al.  Detecting synfire chain activity using massively parallel spike train recording. , 2008, Journal of neurophysiology.

[39]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[40]  Karel Svoboda,et al.  Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice , 2010, Nature.

[41]  A. Thomson,et al.  Interlaminar connections in the neocortex. , 2003, Cerebral cortex.

[42]  K. Harris,et al.  Laminar Structure of Spontaneous and Sensory-Evoked Population Activity in Auditory Cortex , 2009, Neuron.

[43]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[44]  R. Desimone,et al.  Clustering of perirhinal neurons with similar properties following visual experience in adult monkeys , 2000, Nature Neuroscience.

[45]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[46]  A. Seth.  Causal connectivity of evolved neural networks during behavior. , 2005, Network.

[47]  C. Granger.  Investigating causal relations by econometric models and cross-spectral methods , 1969 .

[48]  T. Womelsdorf,et al.  Attentional Stimulus Selection through Selective Synchronization between Monkey Visual Areas , 2012, Neuron.

[49]  David L. Sheinberg,et al.  Visual object recognition. , 1996, Annual review of neuroscience.

[50]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[51]  C. Petersen,et al.  The Excitatory Neuronal Network of the C2 Barrel Column in Mouse Primary Somatosensory Cortex , 2009, Neuron.

[52]  Nicholas J. Priebe,et al.  Mechanisms of Neuronal Computation in Mammalian Visual Cortex , 2012, Neuron.

[53]  Nikos K. Logothetis,et al.  Directed Coupling in Local Field Potentials of Macaque V4 During Visual Short-Term Memory Revealed by Multivariate Autoregressive Models , 2010, Front. Comput. Neurosci..

[54]  Roger Shannon,et al.  Functional connectivity in the pontomedullary respiratory network. , 2008, Journal of neurophysiology.

[55]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

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

[57]  M. A. Smith,et al.  Stimulus Dependence of Neuronal Correlation in Primary Visual Cortex of the Macaque , 2005, The Journal of Neuroscience.

[58]  Mingzhou Ding,et al.  Estimating Granger causality from fourier and wavelet transforms of time series data. , 2007, Physical review letters.

[59]  Rodrigo F. Salazar,et al.  Content-Specific Fronto-Parietal Synchronization During Visual Working Memory , 2012, Science.

[60]  L. Squire,et al.  Neuronal representations of stimulus associations develop in the temporal lobe during learning , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Doris Y. Tsao,et al.  Functional Compartmentalization and Viewpoint Generalization Within the Macaque Face-Processing System , 2010, Science.

[62]  Kenji Kawano,et al.  Global and fine information coded by single neurons in the temporal visual cortex , 1999, Nature.

[63]  S. Gerber,et al.  Unsupervised Natural Experience Rapidly Alters Invariant Object Representation in Visual Cortex , 2008 .

[64]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. I. The single spike train. , 1967, Biophysical journal.

[65]  R. Reid,et al.  The processing and encoding of information in the visual cortex , 1996, Current Opinion in Neurobiology.

[66]  Lee M. Miller,et al.  Feature Selectivity and Interneuronal Cooperation in the Thalamocortical System , 2001, The Journal of Neuroscience.

[67]  R. Reid,et al.  Synchronous activity in the visual system. , 1999, Annual review of physiology.

[68]  Y. Dan,et al.  Spike Timing-Dependent Plasticity of Neural Circuits , 2004, Neuron.

[69]  Boris Gourévitch,et al.  Evaluating information transfer between auditory cortical neurons. , 2007, Journal of neurophysiology.

[70]  Yasushi Miyashita,et al.  Cognitive Memory: Cellular and Network Machineries and Their Top-Down Control , 2004, Science.

[71]  Partha P. Mitra,et al.  Sampling Properties of the Spectrum and Coherency of Sequences of Action Potentials , 2000, Neural Computation.

[72]  Anthony J. Movshon,et al.  Visual Response Properties of Striate Cortical Neurons Projecting to Area MT in Macaque Monkeys , 1996, The Journal of Neuroscience.

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

[74]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[75]  D. Baylor,et al.  Concerted Signaling by Retinal Ganglion Cells , 1995, Science.

[76]  D. Snodderly,et al.  Direction selectivity in V1 of alert monkeys: evidence for parallel pathways for motion processing , 2007, The Journal of physiology.

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

[78]  Thomas D Albright,et al.  On the Perception of Probable Things: Neural Substrates of Associative Memory, Imagery, and Perception , 2012, Neuron.

[79]  T. Wiesel,et al.  Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[80]  C. Gilbert.  Horizontal integration and cortical dynamics , 1992, Neuron.

[81]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[82]  K. Harris.  Neural signatures of cell assembly organization , 2005, Nature Reviews Neuroscience.

[83]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

[84]  G. Buzsáki,et al.  Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex , 2008, Nature Neuroscience.

[85]  Y. Dan,et al.  Activity Recall in Visual Cortical Ensemble , 2012, Nature Neuroscience.

[86]  Craig A. Atencio,et al.  Columnar Connectivity and Laminar Processing in Cat Primary Auditory Cortex , 2010, PloS one.

[87]  Yuji Ikegaya,et al.  Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity , 2004, Science.

[88]  Y. Miyashita,et al.  Functional Microcircuit Recruited during Retrieval of Object Association Memory in Monkey Perirhinal Cortex , 2013, Neuron.

[89]  J. O’Neill,et al.  Play it again: reactivation of waking experience and memory , 2010, Trends in Neurosciences.

[90]  S. Bressler,et al.  Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[91]  R. Desimone,et al.  Responses of Macaque Perirhinal Neurons during and after Visual Stimulus Association Learning , 1999, The Journal of Neuroscience.

[92]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[93]  M. Moser,et al.  Optogenetic Dissection of Entorhinal-Hippocampal Functional Connectivity , 2013, Science.

[94]  R. Silver,et al.  Synaptic connections between layer 4 spiny neurone‐ layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column , 2002, The Journal of physiology.

[95]  J. Csicsvari,et al.  Reliability and State Dependence of Pyramidal Cell–Interneuron Synapses in the Hippocampus an Ensemble Approach in the Behaving Rat , 1998, Neuron.

[96]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[97]  Emilio Salinas,et al.  Transformation of the neural code for tactile detection from thalamus to cortex , 2013, Proceedings of the National Academy of Sciences.

[98]  Rasmus R. Schröder,et al.  Reversal of Interlaminar Signal Between Sensory and Memory Processing in Monkey Temporal Cortex , 2011 .

[99]  G. Buzsáki.  Large-scale recording of neuronal ensembles , 2004, Nature Neuroscience.

[100]  Yasushi Miyashita,et al.  Delay‐period activities in two subdivisions of monkey inferotemporal cortex during pair association memory task , 2003, The European journal of neuroscience.

[101]  P. Goldman-Rakic,et al.  Coding Specificity in Cortical Microcircuits: A Multiple-Electrode Analysis of Primate Prefrontal Cortex , 2001, The Journal of Neuroscience.

[102]  K. Tanaka,et al.  Organization of cat visual cortex as investigated by cross-correlation technique. , 1981, Journal of neurophysiology.

[103]  Bruce L. McNaughton,et al.  The Neurophysiology of Reminiscence , 1998, Neurobiology of Learning and Memory.

[104]  Koichi Sameshima,et al.  Using partial directed coherence to describe neuronal ensemble interactions , 1999, Journal of Neuroscience Methods.

[105]  R. Christopher deCharms,et al.  Primary cortical representation of sounds by the coordination of action-potential timing , 1996, Nature.

[106]  U. Mitzdorf.  Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[107]  A. Lansner.  Associative memory models: from the cell-assembly theory to biophysically detailed cortex simulations , 2009, Trends in Neurosciences.

[108]  Peter Janssen,et al.  Synchronization between the end stages of the dorsal and the ventral visual stream. , 2011, Journal of neurophysiology.

[109]  M. Häusser,et al.  Targeting neurons and photons for optogenetics , 2013, Nature Neuroscience.

[110]  Y. Miyashita,et al.  Backward spreading of memory-retrieval signal in the primate temporal cortex. , 2001, Science.

[111]  R. Desimone,et al.  The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4 , 2008, The Journal of Neuroscience.

[112]  J. Geweke,et al.  Measurement of Linear Dependence and Feedback between Multiple Time Series , 1982 .

[113]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.