Attention-Induced Variance and Noise Correlation Reduction in Macaque V1 Is Mediated by NMDA Receptors

Summary Attention improves perception by affecting different aspects of the neuronal code. It enhances firing rates, it reduces firing rate variability and noise correlations of neurons, and it alters the strength of oscillatory activity. Attention-induced rate enhancement in striate cortex requires cholinergic mechanisms. The neuropharmacological mechanisms responsible for attention-induced variance and noise correlation reduction or those supporting changes in oscillatory activity are unknown. We show that ionotropic glutamatergic receptor activation is required for attention-induced rate variance, noise correlation, and LFP gamma power reduction in macaque V1, but not for attention-induced rate modulations. NMDA receptors mediate attention-induced variance reduction and attention-induced noise correlation reduction. Our results demonstrate that attention improves sensory processing by a variety of mechanisms that are dissociable at the receptor level.

[1]  Peter Dayan,et al.  The Effect of Correlated Variability on the Accuracy of a Population Code , 1999, Neural Computation.

[2]  W. Newsome,et al.  Estimates of the Contribution of Single Neurons to Perception Depend on Timescale and Noise Correlation , 2009, The Journal of Neuroscience.

[3]  Valentin Dragoi,et al.  Adaptive coding of visual information in neural populations , 2008, Nature.

[4]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[5]  Christof Koch,et al.  Visual Saliency Computations: Mechanisms, Constraints, and the Effect of Feedback , 2010, The Journal of Neuroscience.

[6]  Stefan Treue,et al.  Expansion of MT Neurons Excitatory Receptive Fields during Covert Attentive Tracking , 2011, The Journal of Neuroscience.

[7]  Nikos K Logothetis,et al.  Statistical comparison of spike responses to natural stimuli in monkey area V1 with simulated responses of a detailed laminar network model for a patch of V1. , 2011, Journal of neurophysiology.

[8]  M. Sarter,et al.  Bidirectional modulation of basal forebrain N-methyl-d-aspartate receptor function differentially affects visual attention but not visual discrimination performance , 2001, Neuroscience.

[9]  J. Maunsell,et al.  Attention improves performance primarily by reducing interneuronal correlations , 2009, Nature Neuroscience.

[10]  Louise S. Delicato,et al.  Attention Reduces Stimulus-Driven Gamma Frequency Oscillations and Spike Field Coherence in V1 , 2010, Neuron.

[11]  D. Perrett,et al.  The `Ideal Homunculus': decoding neural population signals , 1998, Trends in Neurosciences.

[12]  Xiao-Jing Wang,et al.  Erratum to: Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition , 2014, Journal of Computational Neuroscience.

[13]  P. Goldman-Rakic,et al.  Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. , 2000, Cerebral cortex.

[14]  R. Astur,et al.  Selective Cognitive Impairments Associated with NMDA Receptor Blockade in Humans , 2005, Neuropsychopharmacology.

[15]  J. M. Hupé,et al.  Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons , 1998, Nature.

[16]  Jude F. Mitchell,et al.  Spatial Attention Decorrelates Intrinsic Activity Fluctuations in Macaque Area V4 , 2009, Neuron.

[17]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.

[18]  H. Spitzer,et al.  Increased attention enhances both behavioral and neuronal performance. , 1988, Science.

[19]  D. Goff,et al.  Converging Evidence of NMDA Receptor Hypofunction in the Pathophysiology of Schizophrenia , 2003, Annals of the New York Academy of Sciences.

[20]  Jude F. Mitchell,et al.  Differential Attention-Dependent Response Modulation across Cell Classes in Macaque Visual Area V4 , 2007, Neuron.

[21]  T. Moore,et al.  CONTROL OF VISUAL CORTICAL SIGNALS BY PREFRONTAL DOPAMINE , 2011, Nature.

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

[23]  A. Pouget,et al.  Neural correlations, population coding and computation , 2006, Nature Reviews Neuroscience.

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

[25]  J. Tanji,et al.  Involvement of NMDA and non-NMDA receptors in the neuronal responses of the primary motor cortex to input from the supplementary motor area and somatosensory cortex: studies of task-performing monkeys. , 1998, The Japanese journal of physiology.

[26]  R. Deichmann,et al.  Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex , 2006, Current Biology.

[27]  A. Thiele,et al.  A novel electrode–pipette design for simultaneous recording of extracellular spikes and iontophoretic drug application in awake behaving monkeys , 2006, Journal of Neuroscience Methods.

[28]  Gustavo Deco,et al.  Cholinergic control of cortical network interactions enables feedback‐mediated attentional modulation , 2011, The European journal of neuroscience.

[29]  J. Tanji,et al.  Involvement of NMDA and non-NMDA receptors in motor task-related activity in the primary and secondary cortical motor areas of the monkey. , 1993, Cerebral cortex.

[30]  Xiao-Jing Wang Synaptic reverberation underlying mnemonic persistent activity , 2001, Trends in Neurosciences.

[31]  Matthew W Self,et al.  Different glutamate receptors convey feedforward and recurrent processing in macaque V1 , 2012, Proceedings of the National Academy of Sciences.

[32]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[33]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[34]  Alexander S. Ecker,et al.  Decorrelated Neuronal Firing in Cortical Microcircuits , 2010, Science.

[35]  Andrew M. Clark,et al.  Stimulus onset quenches neural variability: a widespread cortical phenomenon , 2010, Nature Neuroscience.

[36]  R. Traub,et al.  Region-specific changes in gamma and beta2 rhythms in NMDA receptor dysfunction models of schizophrenia. , 2008, Schizophrenia bulletin.

[37]  M. Cohen,et al.  Measuring and interpreting neuronal correlations , 2011, Nature Neuroscience.

[38]  A. Thiele,et al.  Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1 , 2008, The European journal of neuroscience.

[39]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[40]  Valentin Dragoi,et al.  Correlated Variability in Laminar Cortical Circuits , 2012, Neuron.

[41]  A. Thiele,et al.  Attention alters spatial integration in macaque V1 in an eccentricity-dependent manner , 2007, Nature Neuroscience.

[42]  Katherine M. Armstrong,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2003, Nature.

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

[44]  Pieter R. Roelfsema,et al.  Object-based attention in the primary visual cortex of the macaque monkey , 1998, Nature.

[45]  M. Carandini,et al.  Stimulus contrast modulates functional connectivity in visual cortex , 2009, Nature Neuroscience.

[46]  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.

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

[48]  W. Bair,et al.  Correlated Firing in Macaque Visual Area MT: Time Scales and Relationship to Behavior , 2001, The Journal of Neuroscience.

[49]  R. Desimone,et al.  Laminar differences in gamma and alpha coherence in the ventral stream , 2011, Proceedings of the National Academy of Sciences.

[50]  John H. R. Maunsell,et al.  Attentional modulation of visual motion processing in cortical areas MT and MST , 1996, Nature.

[51]  A. Walden,et al.  Spectral analysis for physical applications : multitaper and conventional univariate techniques , 1996 .

[52]  Michael J. Goard,et al.  Basal Forebrain Activation Enhances Cortical Coding of Natural Scenes , 2009, Nature Neuroscience.

[53]  Louise S. Delicato,et al.  Acetylcholine contributes through muscarinic receptors to attentional modulation in V1 , 2008, Nature.

[54]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[55]  Pieter R. Roelfsema,et al.  Noise Correlations Have Little Influence on the Coding of Selective Attention in Area V1 , 2008, Cerebral cortex.