A general decoding strategy explains the relationship between behavior and correlated variability

Increases in perceptual performance correspond to decreases in the correlated variability of sensory neuron responses. No sensory information decoding mechanism has yet explained this relationship. We hypothesize that when observers must respond to a stimulus change of any magnitude, decoders prioritize generality: a single set of neuronal weights to decode any stimulus response. Our mechanistic circuit model supports that a general decoding strategy explains the inverse relationship between perceptual performance and V4 correlated variability observed in two rhesus monkeys performing a visual attention task. Further, based on the recorded V4 population responses, a monkey’s decoding mechanism was more closely matched the more broad the range of stimulus changes used to compute a sensory information decoder. These results support that observers use a general sensory information decoding strategy based on a single set of decoding weights, capable of decoding neuronal responses to the wide variety of stimuli encountered in natural vision.

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

[2]  Byron M. Yu,et al.  Cortical Areas Interact through a Communication Subspace , 2019, Neuron.

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

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

[5]  Amy M. Ni,et al.  Learning and attention reveal a general relationship between population activity and behavior , 2018, Science.

[6]  Thomas Zhihao Luo,et al.  Neuronal Modulations in Visual Cortex Are Associated with Only One of Multiple Components of Attention , 2015, Neuron.

[7]  John H. Reynolds,et al.  Laminar Organization of Attentional Modulation in Macaque Visual Area V4 , 2017, Neuron.

[8]  Sophie Deneve,et al.  Making Decisions with Unknown Sensory Reliability , 2012, Front. Neurosci..

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

[10]  Amy M. Ni,et al.  Cognition as a Window into Neuronal Population Space. , 2018, Annual review of neuroscience.

[11]  Eero P. Simoncelli,et al.  Partitioning neuronal variability , 2014, Nature Neuroscience.

[12]  Si Wu,et al.  Perceptual training continuously refines neuronal population codes in primary visual cortex , 2014, Nature Neuroscience.

[13]  Lindsey L. Glickfeld,et al.  Neuronal Adaptation Reveals a Suboptimal Decoding of Orientation Tuned Populations in the Mouse Visual Cortex , 2018, The Journal of Neuroscience.

[14]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[15]  Robert Desimone,et al.  Lesions of prefrontal cortex reduce attentional modulation of neuronal responses and synchrony in V4 , 2014, Nature Neuroscience.

[16]  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.

[17]  Alexandre Zénon,et al.  Attention deficits without cortical neuronal deficits , 2012, Nature.

[18]  Alexandre Pouget,et al.  Origin of information-limiting noise correlations , 2015, Proceedings of the National Academy of Sciences.

[19]  R. F. Wagner,et al.  Efficiency of human visual signal discrimination. , 1981, Science.

[20]  Richard E. Turner,et al.  A Structured Model of Video Reproduces Primary Visual Cortical Organisation , 2009, PLoS Comput. Biol..

[21]  M. Bethge,et al.  Inferring decoding strategies from choice probabilities in the presence of correlated variability , 2013, Nature Neuroscience.

[22]  Jeannette A. M. Lorteije,et al.  The Formation of Hierarchical Decisions in the Visual Cortex , 2015, Neuron.

[23]  Haim Sompolinsky,et al.  Implications of Neuronal Diversity on Population Coding , 2006, Neural Computation.

[24]  D. Coppola,et al.  Universality in the Evolution of Orientation Columns in the Visual Cortex , 2010, Science.

[25]  J. Maunsell,et al.  Graded Neuronal Modulations Related to Visual Spatial Attention , 2016, The Journal of Neuroscience.

[26]  Douglas A Ruff,et al.  Stimulus Dependence of Correlated Variability across Cortical Areas , 2016, The Journal of Neuroscience.

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

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

[29]  Brent Doiron,et al.  Scaling Properties of Dimensionality Reduction for Neural Populations and Network Models , 2016, PLoS Comput. Biol..

[30]  J. Maunsell,et al.  Attention-related changes in correlated neuronal activity arise from normalization mechanisms , 2017, Nature Neuroscience.

[31]  Brent Doiron,et al.  Attentional modulation of neuronal variability in circuit models of cortex , 2017, eLife.

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

[33]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

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

[35]  D. Kersten Statistical efficiency for the detection of visual noise , 1987, Vision Research.

[36]  Alexandre Pouget,et al.  Measuring Fisher Information Accurately in Correlated Neural Populations , 2015, PLoS Comput. Biol..

[37]  Brent Doiron,et al.  Circuit-based models of shared variability in cortical networks , 2017, bioRxiv.

[38]  Douglas A Ruff,et al.  Global Cognitive Factors Modulate Correlated Response Variability between V4 Neurons , 2014, The Journal of Neuroscience.

[39]  Yong Gu,et al.  Perceptual Learning Reduces Interneuronal Correlations in Macaque Visual Cortex , 2011, Neuron.

[40]  Byron M. Yu,et al.  Dimensionality reduction for large-scale neural recordings , 2014, Nature Neuroscience.

[41]  D. C. Howell Statistical Methods for Psychology , 1987 .

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

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

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

[45]  Douglas A Ruff,et al.  Simultaneous multi-area recordings suggest that attention improves performance by reshaping stimulus representations , 2019, Nature Neuroscience.

[46]  B. Cumming,et al.  Decision-Related Activity in Macaque V2 for Fine Disparity Discrimination Is Not Compatible with Optimal Linear Readout , 2017, The Journal of Neuroscience.

[47]  Brent Doiron,et al.  Circuit Models of Low-Dimensional Shared Variability in Cortical Networks , 2019, Neuron.

[48]  P. Latham,et al.  Cracking the Neural Code for Sensory Perception by Combining Statistics, Intervention, and Behavior , 2017, Neuron.

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

[50]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[51]  Sheila Nirenberg,et al.  Decoding neuronal spike trains: How important are correlations? , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Alexandre Pouget,et al.  Internally generated population activity in cortical networks hinders information transmission , 2020, bioRxiv.