A neural correlate of visual feature binding in primate lateral prefrontal cortex

We effortlessly perceive visual objects as unified entities, despite the preferential encoding of their various visual features in separate cortical areas. A 'binding' process is assumed to be required for creating this unified percept, but the underlying neural mechanism and specific brain areas are poorly understood. We investigated 'feature-binding' across two feature dimensions, using a novel stimulus configuration, designed to disambiguate whether a given combination of color and motion direction is perceived as bound or unbound. In the "bound" condition, two behaviorally relevant features (color and motion) belong to the same object, while in the "unbound" condition they belong to different objects. We recorded local field potentials from the lateral prefrontal cortex (lPFC) in macaque monkeys that actively monitored the different stimulus configurations. Our data show a neural representation of visual feature binding especially in the 4-12Hz frequency band and a transmission of binding information between different lPFC neural subpopulations. This information is linked to the animal's reaction time, suggesting a behavioral relevance of the binding information. Together, our results document the involvement of the prefrontal cortex, targeted by the dorsal and ventral visual streams, in binding visual features from different dimensions, in a process that includes a dynamic modulation of low frequency inter-regional communication.

[1]  R. Desimone,et al.  Neural Mechanisms of Object-Based Attention , 2014, Science.

[2]  Hans-Jochen Heinze,et al.  Object-based attention involves the sequential activation of feature-specific cortical modules , 2014, Nature Neuroscience.

[3]  Nao Ninomiya,et al.  The 10th anniversary of journal of visualization , 2007, J. Vis..

[4]  Paul H. E. Tiesinga,et al.  Top-down control of cortical gamma-band communication via pulvinar induced phase shifts in the alpha rhythm , 2017, PLoS Comput. Biol..

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

[6]  Bernhard Schölkopf,et al.  Shifts of Gamma Phase across Primary Visual Cortical Sites Reflect Dynamic Stimulus-Modulated Information Transfer , 2015, PLoS biology.

[7]  Gustavo Deco,et al.  Neuronal Discharges and Gamma Oscillations Explicitly Reflect Visual Consciousness in the Lateral Prefrontal Cortex , 2012, Neuron.

[8]  D. Whitney.  Neuroscience: Toward Unbinding the Binding Problem , 2009, Current Biology.

[9]  John C Gore,et al.  The role of the parietal cortex in visual feature binding , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Stefan Treue,et al.  Saccade-synchronized rapid attention shifts in macaque visual cortical area MT , 2018, Nature Communications.

[11]  Huan Luo,et al.  The causal role of α-oscillations in feature binding , 2019, Proceedings of the National Academy of Sciences.

[12]  Mohammad Reza Daliri,et al.  Single-Trial Decoding from Local Field Potential Using Bag of Word Representation , 2019, Brain Topography.

[13]  David A. Nipperess,et al.  Conservation prioritization can resolve the flagship species conundrum , 2020, Nature Communications.

[14]  T. Stanford,et al.  Development of multisensory integration from the perspective of the individual neuron , 2014, Nature Reviews Neuroscience.

[15]  S. Thorpe,et al.  The Time Course of Visual Processing: From Early Perception to Decision-Making , 2001, Journal of Cognitive Neuroscience.

[16]  J. Tanji,et al.  Integration of temporal order and object information in the monkey lateral prefrontal cortex. , 2004, Journal of neurophysiology.

[17]  R. Desimone,et al.  The Role of Neural Mechanisms of Attention in Solving the Binding Problem , 1999, Neuron.

[18]  S Treue,et al.  Standardized automated training of rhesus monkeys for neuroscience research in their housing environment. , 2018, Journal of neurophysiology.

[19]  Sébastien M. Crouzet,et al.  Fast saccades toward faces: face detection in just 100 ms. , 2010, Journal of vision.

[20]  J. D. E. Gabrieli,et al.  Integration of diverse information in working memory within the frontal lobe , 2000, Nature Neuroscience.

[21]  Hassan,et al.  Does , 2020, The Goat.

[22]  S. Treue,et al.  Commentary: The causal role of α-oscillations in feature binding , 2020, Frontiers in Neuroscience.

[23]  S. Treue,et al.  Basic Neuroscience Research with Nonhuman Primates: A Small but Indispensable Component of Biomedical Research , 2014, Neuron.

[24]  Mohammad Reza Daliri,et al.  Decoding of Visual Attention from LFP Signals of Macaque MT , 2014, PloS one.

[25]  Andreas Bartels,et al.  The Coding of Color, Motion, and Their Conjunction in the Human Visual Cortex , 2009, Current Biology.

[26]  Stefan Treue,et al.  Feature-based attentional integration of color and visual motion. , 2006, Journal of vision.

[27]  Guillaume A. Rousselet,et al.  Parallel processing in high-level categorization of natural images , 2002, Nature Neuroscience.

[28]  T. Poggio,et al.  Object Selectivity of Local Field Potentials and Spikes in the Macaque Inferior Temporal Cortex , 2006, Neuron.

[29]  S. Treue,et al.  Electrical stimulation of macaque lateral prefrontal cortex modulates oculomotor behavior indicative of a disruption of top-down attention , 2017, Scientific Reports.

[30]  Kazuyuki Aihara,et al.  Solving the binding problem of the brain with bi-directional functional connectivity , 2001, Neural Networks.

[31]  R. Born,et al.  Integrating motion and depth via parallel pathways , 2008, Nature Neuroscience.

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

[33]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[34]  A. Treisman,et al.  Illusory conjunctions in the perception of objects , 1982, Cognitive Psychology.

[35]  Mohammad Reza Daliri,et al.  Neural Activity Predicts Reaction in Primates Long Before a Behavioral Response , 2018, Front. Behav. Neurosci..

[36]  S. Treue,et al.  The lateral prefrontal cortex of primates encodes stimulus colors and their behavioral relevance during a match-to-sample task , 2020, Scientific Reports.

[37]  J. Maunsell,et al.  Differences in Gamma Frequencies across Visual Cortex Restrict Their Possible Use in Computation , 2010, Neuron.

[38]  F. Tong,et al.  Neural mechanisms of object-based attention. , 2015, Cerebral cortex.

[39]  L. Robertson.  Binding, spatial attention and perceptual awareness , 2003, Nature Reviews Neuroscience.

[40]  Rüdiger von der Heydt,et al.  Spike Synchrony Reveals Emergence of Proto-Objects in Visual Cortex , 2015, The Journal of Neuroscience.

[41]  H. Müller,et al.  Synchronous Information Presented in 40-HZ Flicker Enhances Visual Feature Binding , 1998 .

[42]  Sang Wook Hong,et al.  Misbinding of color to form in afterimages , 2008, Visual Neuroscience.

[43]  P. Roelfsema,et al.  Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex , 2014, Proceedings of the National Academy of Sciences.

[44]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[45]  A. Treisman,et al.  Parietal contributions to visual feature binding: evidence from a patient with bilateral lesions , 1995, Science.

[46]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[47]  Mohammad Reza Daliri,et al.  Attention decouples action potentials from the phase of local field potentials in macaque visual cortical area MT , 2018, BMC Biology.

[48]  C. Granger.  Investigating Causal Relations by Econometric Models and Cross-Spectral Methods , 1969 .

[49]  G. Humphreys,et al.  The role of reentrant processes in feature binding: Evidence from neuropsychology and TMS on late onset illusory conjunctions , 2009 .

[50]  D. Leopold,et al.  Layer-Specific Entrainment of Gamma-Band Neural Activity by the Alpha Rhythm in Monkey Visual Cortex , 2012, Current Biology.

[51]  A. Thiele,et al.  Neuronal synchrony does not correlate with motion coherence in cortical area MT , 2003, Nature.

[52]  Michael N. Shadlen,et al.  Synchrony Unbound A Critical Evaluation of the Temporal Binding Hypothesis , 1999, Neuron.

[53]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[54]  Nancy Kanwisher,et al.  Feature-Binding Errors After Eye Movements and Shifts of Attention , 2014, Psychological science.

[55]  S. Treue,et al.  Strategic deployment of feature-based attentional gain in primate visual cortex , 2019, PLoS biology.

[56]  C. Metz.  Basic principles of ROC analysis. , 1978, Seminars in nuclear medicine.

[57]  Robert Desimone,et al.  Pulvinar-Cortex Interactions in Vision and Attention , 2016, Neuron.

[58]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[59]  Charles E. Davis,et al.  Zapping 500 faces in less than 100 seconds: Evidence for extremely fast and sustained continuous visual search , 2018, Scientific Reports.

[60]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[61]  Stefan Treue,et al.  Attention strengthens across-trial pre-stimulus phase coherence in visual cortex, enhancing stimulus processing , 2020, Scientific Reports.

[62]  G. DeAngelis,et al.  Does Neuronal Synchrony Underlie Visual Feature Grouping? , 2005, Neuron.

[63]  Anil K. Seth,et al.  The MVGC multivariate Granger causality toolbox: A new approach to Granger-causal inference , 2014, Journal of Neuroscience Methods.

[64]  Christoph von der Malsburg,et al.  The Correlation Theory of Brain Function , 1994 .

[65]  Fang Fang,et al.  Misbinding of Color and Motion in Human Visual Cortex , 2014, Current Biology.

[66]  T D Albright,et al.  The Contribution of Color to Motion Processing in Macaque Middle Temporal Area , 1999, The Journal of Neuroscience.

[67]  C. Landry,et al.  A systems biology approach to explore the impact of maple tree dormancy release on sap variation and maple syrup quality , 2018, Scientific Reports.

[68]  Stefan Treue,et al.  Attention amplifies neural representations of changes in sensory input at the expense of perceptual accuracy , 2020, Nature Communications.

[69]  Hui Sun Leong,et al.  Longitudinal single-cell RNA sequencing of patient-derived primary cells reveals drug-induced infidelity in stem cell hierarchy , 2018, Nature Communications.

[70]  S. Treue,et al.  Local field potentials are induced by visually evoked spiking activity in macaque cortical area MT , 2017, Scientific Reports.

[71]  Bevil R. Conway,et al.  Toward a Unified Theory of Visual Area V4 , 2012, Neuron.

[72]  H. Kennedy,et al.  Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas , 2016, Neuron.

[73]  Semir Zeki,et al.  Feature binding in the feedback layers of area V2. , 2009, Cerebral cortex.

[74]  Haluk Öğmen,et al.  Perceptual grouping induces non-retinotopic feature attribution in human vision , 2006, Vision Research.

[75]  Stefan Treue,et al.  Spatial Attention Reduces Burstiness in Macaque Visual Cortical Area MST , 2016, Cerebral cortex.

[76]  Shinsuke Shimojo,et al.  Vision: Steady-state misbinding of colour and motion , 2004, Nature.

[77]  J-M Hopf,et al.  Dynamics of feature binding during object-selective attention , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[78]  S. Treue,et al.  Assessment of stress responses in rhesus macaques (Macaca mulatta) to daily routine procedures in system neuroscience based on salivary cortisol concentrations , 2018, PloS one.

[79]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[80]  A. Gail,et al.  A cage-based training, cognitive testing and enrichment system optimized for rhesus macaques in neuroscience research , 2017, Behavior research methods.