Task-dependent representations of stimulus and choice in mouse parietal cortex

The posterior parietal cortex (PPC) has been implicated in perceptual decisions, but whether its role is specific to sensory processing or sensorimotor transformation is not well understood. To distinguish these possibilities, we trained mice of either sex to perform a visual discrimination task and imaged the activity of PPC populations during both engaged behavior and passive viewing. Unlike neurons in primary visual cortex (V1), which responded robustly to stimuli in both conditions, most neurons in PPC responded exclusively during task engagement. However, PPC responses were heterogeneous, with a smaller subset of neurons exhibiting stimulus-driven, contrast-dependent responses in both conditions. Neurons in PPC also exhibit stronger modulation by noise correlations relative to V1, as illustrated by a generalized linear model that takes into account both task variables and between-neuron correlations. To test whether PPC responses primarily encoded the stimulus or the learned sensorimotor contingency, we imaged the same neurons before and after re-training mice on a reversed task contingency. Unlike V1 neurons, most PPC neurons exhibited a dramatic shift in selectivity after re-training and reflected the new sensorimotor contingency, while a smaller subset of neurons preserved their stimulus selectivity. Mouse PPC is therefore strongly task-dependent, contains heterogeneous populations sensitive to stimulus and choice, and may play an important role in the flexible transformation of sensory inputs into motor commands. Significance Statement Perceptual decision making involves both processing of sensory information and mapping that information onto appropriate motor commands via learned sensorimotor associations. While visual cortex (V1) is known to be critical for sensory processing, it is unclear what circuits are involved in the process of sensorimotor transformation. While the mouse posterior parietal cortex (PPC) has been implicated in visual decisions, its specific role has been controversial. By imaging population activity while manipulating task engagement and sensorimotor contingencies, we demonstrate that PPC, unlike V1, is highly task-dependent, heterogeneous, and sensitive to the learned task demands. Our results suggest that PPC is more than a visual area, and may instead be involved in the flexible mapping of visual information onto appropriate motor actions.

[1]  Ian Nauhaus,et al.  Topography and Areal Organization of Mouse Visual Cortex , 2014, The Journal of Neuroscience.

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

[3]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[4]  K. H. Britten,et al.  A relationship between behavioral choice and the visual responses of neurons in macaque MT , 1996, Visual Neuroscience.

[5]  B. Hangya,et al.  Distinct behavioural and network correlates of two interneuron types in prefrontal cortex , 2013, Nature.

[6]  Zengcai V. Guo,et al.  A motor cortex circuit for motor planning and movement , 2015, Nature.

[7]  Somnath Datta,et al.  A Signed‐Rank Test for Clustered Data , 2008, Biometrics.

[8]  Olaf Sporns,et al.  Network Analysis of Corticocortical Connections Reveals Ventral and Dorsal Processing Streams in Mouse Visual Cortex , 2012, The Journal of Neuroscience.

[9]  R. L. Reep,et al.  Rat posterior parietal cortex: topography of corticocortical and thalamic connections , 2004, Experimental Brain Research.

[10]  Eero P. Simoncelli,et al.  Spatio-temporal correlations and visual signalling in a complete neuronal population , 2008, Nature.

[11]  Matthew T. Kaufman,et al.  Posterior Parietal Cortex Guides Visual Decisions in Rats , 2016, The Journal of Neuroscience.

[12]  J. Movshon,et al.  Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex , 1997, The Journal of Neuroscience.

[13]  Emery N. Brown,et al.  Denoising Two-Photon Calcium Imaging Data , 2011, PloS one.

[14]  F. Helmchen,et al.  Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex , 2013, Nature.

[15]  Ari S. Morcos,et al.  History-dependent variability in population dynamics during evidence accumulation in cortex , 2016, Nature Neuroscience.

[16]  Mitra Javadzadeh,et al.  Long-range population dynamics of anatomically defined neocortical networks , 2016, eLife.

[17]  Hongkui Zeng,et al.  Differential tuning and population dynamics of excitatory and inhibitory neurons reflect differences in local intracortical connectivity , 2011, Nature Neuroscience.

[18]  M. Carandini,et al.  Probing perceptual decisions in rodents , 2013, Nature Neuroscience.

[19]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

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

[21]  Uri T Eden,et al.  A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. , 2005, Journal of neurophysiology.

[22]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[23]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[24]  R. Romo,et al.  Decoding a Perceptual Decision Process across Cortex , 2010, Neuron.

[25]  Mriganka Sur,et al.  Spatial Correlations in Natural Scenes Modulate Response Reliability in Mouse Visual Cortex , 2015, The Journal of Neuroscience.

[26]  Yang Dan,et al.  Cell-Type-Specific Activity in Prefrontal Cortex during Goal-Directed Behavior , 2015, Neuron.

[27]  David J. Freedman,et al.  Biased Associative Representations in Parietal Cortex , 2013, Neuron.

[28]  Matthew T. Kaufman,et al.  A category-free neural population supports evolving demands during decision-making , 2014, Nature Neuroscience.

[29]  Zengcai V. Guo,et al.  Flow of Cortical Activity Underlying a Tactile Decision in Mice , 2014, Neuron.

[30]  Somnath Datta,et al.  Rank-Sum Tests for Clustered Data , 2005 .

[31]  David W. Tank,et al.  Regression-Based Identification of Behavior-Encoding Neurons During Large-Scale Optical Imaging of Neural Activity at Cellular Resolution , 2010, Journal of neurophysiology.

[32]  James H. Marshel,et al.  Functional Specialization of Seven Mouse Visual Cortical Areas , 2011, Neuron.

[33]  Bingni W. Brunton,et al.  Distinct relationships of parietal and prefrontal cortices to evidence accumulation , 2014, Nature.

[34]  Mriganka Sur,et al.  Distinct roles of visual, parietal, and frontal motor cortices in memory-guided sensorimotor decisions , 2016, eLife.

[35]  Matthijs Verhage,et al.  A solution to dependency: using multilevel analysis to accommodate nested data , 2014, Nature Neuroscience.

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

[37]  Jessica A. Cardin,et al.  Projection-Specific Visual Feature Encoding by Layer 5 Cortical Subnetworks. , 2016, Cell reports.

[38]  Michael J. Goard,et al.  Fast Modulation of Visual Perception by Basal Forebrain Cholinergic Neurons , 2013, Nature Neuroscience.

[39]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[40]  Jay A. Hennig,et al.  Signal Multiplexing and Single-Neuron Computations in Lateral Intraparietal Area During Decision-Making , 2013, The Journal of Neuroscience.

[41]  Bingni W. Brunton,et al.  Distinct effects of prefrontal and parietal cortex inactivations on an accumulation of evidence task in the rat , 2015, bioRxiv.

[42]  D. R. Muir,et al.  Functional organization of excitatory synaptic strength in primary visual cortex , 2015, Nature.

[43]  David J. Freedman,et al.  Experience-dependent representation of visual categories in parietal cortex , 2006, Nature.

[44]  R. Reid,et al.  Frontiers in Cellular Neuroscience Cellular Neuroscience Methods Article , 2022 .

[45]  Quanxin Wang,et al.  Area map of mouse visual cortex , 2007, The Journal of comparative neurology.

[46]  Christopher D. Harvey,et al.  Choice-specific sequences in parietal cortex during a virtual-navigation decision task , 2012, Nature.

[47]  J. Simon Wiegert,et al.  Multiple dynamic representations in the motor cortex during sensorimotor learning , 2012, Nature.

[48]  Sally Galbraith,et al.  A Study of Clustered Data and Approaches to Its Analysis , 2010, The Journal of Neuroscience.

[49]  J. Gold,et al.  Distinct Representations of a Perceptual Decision and the Associated Oculomotor Plan in the Monkey Lateral Intraparietal Area , 2011, The Journal of Neuroscience.

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

[51]  D. G. Albrecht,et al.  Striate cortex of monkey and cat: contrast response function. , 1982, Journal of neurophysiology.

[52]  L. Giovannelli,et al.  The central cholinergic system during aging. , 1994, Progress in brain research.

[53]  W. Newsome,et al.  Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. , 2001, Journal of neurophysiology.

[54]  Jack L. Gallant,et al.  A Continuous Semantic Space Describes the Representation of Thousands of Object and Action Categories across the Human Brain , 2012, Neuron.