Attentional modulation of neuronal variability in circuit models of cortex

The circuit mechanisms behind shared neural variability (noise correlation) and its dependence on neural state are poorly understood. Visual attention is well-suited to constrain cortical models of response variability because attention both increases firing rates and their stimulus sensitivity, as well as decreases noise correlations. We provide a novel analysis of population recordings in rhesus primate visual area V4 showing that a single biophysical mechanism may underlie these diverse neural correlates of attention. We explore model cortical networks where top-down mediated increases in excitability, distributed across excitatory and inhibitory targets, capture the key neuronal correlates of attention. Our models predict that top-down signals primarily affect inhibitory neurons, whereas excitatory neurons are more sensitive to stimulus specific bottom-up inputs. Accounting for trial variability in models of state dependent modulation of neuronal activity is a critical step in building a mechanistic theory of neuronal cognition. DOI: http://dx.doi.org/10.7554/eLife.23978.001

[1]  C. Gilbert,et al.  Brain States: Top-Down Influences in Sensory Processing , 2007, Neuron.

[2]  S. Treue Neural correlates of attention in primate visual cortex , 2001, Trends in Neurosciences.

[3]  Evan S. Schaffer,et al.  Inhibitory Stabilization of the Cortical Network Underlies Visual Surround Suppression , 2009, Neuron.

[4]  Maneesh Sahani,et al.  Inhibitory control of correlated intrinsic variability in cortical networks , 2016 .

[5]  K. Deisseroth,et al.  Prefrontal Parvalbumin Neurons in Control of Attention , 2016, Cell.

[6]  Alexander S. Ecker,et al.  On the structure of population activity under fluctuations in attentional state , 2015 .

[7]  John H Reynolds,et al.  Muscarinic acetylcholine receptors are expressed by most parvalbumin-immunoreactive neurons in area MT of the macaque , 2014, Brain and behavior.

[8]  J. Poulet,et al.  Synaptic Mechanisms Underlying Sparse Coding of Active Touch , 2011, Neuron.

[9]  Eero P. Simoncelli,et al.  Attention stabilizes the shared gain of V4 populations , 2015, eLife.

[10]  Jessica A. Cardin,et al.  Stimulus Feature Selectivity in Excitatory and Inhibitory Neurons in Primary Visual Cortex , 2007, The Journal of Neuroscience.

[11]  M. A. Smith,et al.  The spatial structure of correlated neuronal variability , 2016, Nature Neuroscience.

[12]  P. Tiesinga,et al.  Role of interneuron diversity in the cortical microcircuit for attention. , 2008, Journal of neurophysiology.

[13]  M. Scanziani,et al.  How Inhibition Shapes Cortical Activity , 2011, Neuron.

[14]  Cheng Ly,et al.  Cellular and Circuit Mechanisms Maintain Low Spike Co-Variability and Enhance Population Coding in Somatosensory Cortex , 2012, Front. Comput. Neurosci..

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

[16]  Johannes J. Letzkus,et al.  Cholinergic circuit modulation through differential recruitment of neocortical interneuron types during behaviour , 2014, The Journal of physiology.

[17]  Eric Shea-Brown,et al.  From the statistics of connectivity to the statistics of spike times in neuronal networks , 2017, Current Opinion in Neurobiology.

[18]  G. Fishell,et al.  A disinhibitory circuit mediates motor integration in the somatosensory cortex , 2013, Nature Neuroscience.

[19]  M. Hasselmo Neuromodulation and cortical function: modeling the physiological basis of behavior , 1995, Behavioural Brain Research.

[20]  Alexander S. Ecker,et al.  On the Structure of Neuronal Population Activity under Fluctuations in Attentional State , 2015, The Journal of Neuroscience.

[21]  Y. Dan,et al.  Neuromodulation of Brain States , 2012, Neuron.

[22]  A. Pouget,et al.  Information-limiting correlations , 2014, Nature Neuroscience.

[23]  K. Harris,et al.  Cortical state and attention , 2011, Nature Reviews Neuroscience.

[24]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

[25]  Douglas A Ruff,et al.  Attention can increase or decrease spike count correlations between pairs of neurons depending on their role in a task , 2014, Nature Neuroscience.

[26]  Tai Sing Lee,et al.  Local field potentials indicate network state and account for neuronal response variability , 2010, Journal of Computational Neuroscience.

[27]  Eric Shea-Brown,et al.  Impact of Network Structure and Cellular Response on Spike Time Correlations , 2011, PLoS Comput. Biol..

[28]  Yang Dan,et al.  Cell-type-specific modulation of neocortical activity by basal forebrain input , 2013, Front. Syst. Neurosci..

[29]  L. Itti,et al.  Modeling the influence of task on attention , 2005, Vision Research.

[30]  C. Distler,et al.  Attention and normalization circuits in macaque V1 , 2015, The European journal of neuroscience.

[31]  C. W. Gardiner,et al.  Handbook of stochastic methods - for physics, chemistry and the natural sciences, Second Edition , 1986, Springer series in synergetics.

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

[33]  A. Pouget,et al.  Correlations and Neuronal Population Information. , 2016, Annual review of neuroscience.

[34]  Moritz Helias,et al.  The Correlation Structure of Local Neuronal Networks Intrinsically Results from Recurrent Dynamics , 2013, PLoS Comput. Biol..

[35]  G. Fishell,et al.  Interneuron cell types are fit to function , 2014, Nature.

[36]  Grace W. Lindsay,et al.  Parallel processing by cortical inhibition enables context-dependent behavior , 2016, Nature Neuroscience.

[37]  P. Dayan,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S9 References the Asynchronous State in Cortical Circuits , 2022 .

[38]  Brent Doiron,et al.  Oscillatory activity in electrosensory neurons increases with the spatial correlation of the stochastic input stimulus. , 2004, Physical review letters.

[39]  M. Scanziani,et al.  Inhibition of Inhibition in Visual Cortex: The Logic of Connections Between Molecularly Distinct Interneurons , 2013, Nature Neuroscience.

[40]  Xiao-Jing Wang,et al.  An Integrated Microcircuit Model of Attentional Processing in the Neocortex , 2007, The Journal of Neuroscience.

[41]  Haim Sompolinsky,et al.  Chaotic Balanced State in a Model of Cortical Circuits , 1998, Neural Computation.

[42]  Brent Doiron,et al.  The mechanics of state-dependent neural correlations , 2016, Nature Neuroscience.

[43]  M. Stryker,et al.  A Cortical Circuit for Gain Control by Behavioral State , 2014, Cell.

[44]  Alexander Thiele,et al.  Attention-Induced Variance and Noise Correlation Reduction in Macaque V1 Is Mediated by NMDA Receptors , 2013, Neuron.

[45]  Alexander S. Ecker,et al.  State Dependence of Noise Correlations in Macaque Primary Visual Cortex , 2014, Neuron.

[46]  Alexandre Pouget,et al.  Insights from a Simple Expression for Linear Fisher Information in a Recurrently Connected Population of Spiking Neurons , 2011, Neural Computation.

[47]  T. Moore,et al.  The role of neuromodulators in selective attention , 2011, Trends in Cognitive Sciences.

[48]  J. Maunsell,et al.  Attention to both space and feature modulates neuronal responses in macaque area V4. , 2000, Journal of neurophysiology.

[49]  J. Maunsell,et al.  Using Neuronal Populations to Study the Mechanisms Underlying Spatial and Feature Attention , 2011, Neuron.

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

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

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

[53]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[54]  M. Carandini,et al.  The Nature of Shared Cortical Variability , 2015, Neuron.

[55]  M. Hawken,et al.  Gain Modulation by Nicotine in Macaque V1 , 2007, Neuron.

[56]  Nicolas Brunel,et al.  Dynamics of Networks of Excitatory and Inhibitory Neurons in Response to Time-Dependent Inputs , 2011, Front. Comput. Neurosci..

[57]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[58]  Gianluigi Mongillo,et al.  Bistability and spatiotemporal irregularity in neuronal networks with nonlinear synaptic transmission. , 2012, Physical review letters.

[59]  Tatiana A. Engel,et al.  Selective modulation of cortical state during spatial attention , 2016, Science.

[60]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[61]  Daniel B. Rubin,et al.  The Stabilized Supralinear Network: A Unifying Circuit Motif Underlying Multi-Input Integration in Sensory Cortex , 2015, Neuron.

[62]  Stefan Rotter,et al.  How Structure Determines Correlations in Neuronal Networks , 2011, PLoS Comput. Biol..

[63]  Sompolinsky,et al.  Theory of correlations in stochastic neural networks. , 1994, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[64]  Matthew R Whiteway,et al.  Revealing unobserved factors underlying cortical activity using a rectified latent variable model applied to neural population recordings , 2016, bioRxiv.

[65]  J. Maunsell,et al.  Effects of spatial attention on contrast response functions in macaque area V4. , 2006, Journal of neurophysiology.

[66]  G. Fishell,et al.  Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons , 2011, Developmental neurobiology.

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

[68]  Multiplying two numbers together in your head is a difficult task if you did not learn multiplication tables as a child. On the face of it, this is somewhat surprising given the remarkable power of the brain to perform , 2010 .

[69]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

[70]  Brent Doiron,et al.  Feedback-induced gain control in stochastic spiking networks , 2009, Biological Cybernetics.

[71]  Moritz Helias,et al.  Decorrelation of Neural-Network Activity by Inhibitory Feedback , 2012, PLoS Comput. Biol..

[72]  H. Sompolinsky,et al.  Theory of orientation tuning in visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[73]  T. Tsumoto,et al.  GABAergic Neurons Are Less Selective to Stimulus Orientation than Excitatory Neurons in Layer II/III of Visual Cortex, as Revealed by In Vivo Functional Ca2+ Imaging in Transgenic Mice , 2007, The Journal of Neuroscience.

[74]  Alexander S. Ecker,et al.  Generating Spike Trains with Specified Correlation Coefficients , 2009, Neural Computation.