Projection-Specific Visual Feature Encoding by Layer 5 Cortical Subnetworks.

Primary neocortical sensory areas act as central hubs, distributing afferent information to numerous cortical and subcortical structures. However, it remains unclear whether each downstream target receives a distinct version of sensory information. We used in vivo calcium imaging combined with retrograde tracing to monitor visual response properties of three distinct subpopulations of projection neurons in primary visual cortex. Although there is overlap across the groups, on average, corticotectal (CT) cells exhibit lower contrast thresholds and broader tuning for orientation and spatial frequency in comparison to corticostriatal (CS) cells, whereas corticocortical (CC) cells have intermediate properties. Noise correlational analyses support the hypothesis that CT cells integrate information across diverse layer 5 populations, whereas CS and CC cells form more selectively interconnected groups. Overall, our findings demonstrate the existence of functional subnetworks within layer 5 that may differentially route visual information to behaviorally relevant downstream targets.

[1]  Bernardo L. Sabatini,et al.  Competitive regulation of synaptic Ca influx by D2 dopamine and A2A adenosine receptors , 2010, Nature Neuroscience.

[2]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  Karel Svoboda,et al.  ScanImage: Flexible software for operating laser scanning microscopes , 2003, Biomedical engineering online.

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

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

[6]  W. M. Keck,et al.  Highly Selective Receptive Fields in Mouse Visual Cortex , 2008, The Journal of Neuroscience.

[7]  B. Sabatini,et al.  Calcium Signaling in Dendrites and Spines: Practical and Functional Considerations , 2008, Neuron.

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

[9]  L. Palmer,et al.  Response to Contrast of Electrophysiologically Defined Cell Classes in Primary Visual Cortex , 2003, The Journal of Neuroscience.

[10]  D. Ringach,et al.  On the classification of simple and complex cells , 2002, Vision Research.

[11]  N. Laird,et al.  Meta-analysis in clinical trials. , 1986, Controlled clinical trials.

[12]  Li I. Zhang,et al.  Synaptic Mechanisms Underlying Functional Dichotomy between Intrinsic-Bursting and Regular-Spiking Neurons in Auditory Cortical Layer 5 , 2013, The Journal of Neuroscience.

[13]  R. Douglas,et al.  Characterization of mouse cortical spatial vision , 2004, Vision Research.

[14]  M. A. Smith,et al.  Spatial and Temporal Scales of Neuronal Correlation in Primary Visual Cortex , 2008, The Journal of Neuroscience.

[15]  B. Sabatini,et al.  A Direct Projection from Mouse Primary Visual Cortex to Dorsomedial Striatum , 2014, PloS one.

[16]  J Anthony Movshon,et al.  Visual Response Properties of V1 Neurons Projecting to V2 in Macaque , 2013, The Journal of Neuroscience.

[17]  S. Nelson,et al.  Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. , 2007, Journal of neurophysiology.

[18]  BsnNr C. Srorn,et al.  CLASSIFYING SIMPLE AND COMPLEX CELLS ON THE BASIS OF RESPONSE MODULATION , 2002 .

[19]  Ho Ko,et al.  Emergence of Feature-Specific Connectivity in Cortical Microcircuits in the Absence of Visual Experience , 2014, The Journal of Neuroscience.

[20]  W. G. Cochran Problems arising in the analysis of a series of similar experiments , 1937 .

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

[22]  P. Dean,et al.  Head and body movements produced by electrical stimulation of superior colliculus in rats: Effects of interruption of crossed tectoreticulospinal pathway , 1986, Neuroscience.

[23]  E. Callaway,et al.  Three Types of Cortical Layer 5 Neurons That Differ in Brain-wide Connectivity and Function , 2015, Neuron.

[24]  Emery N. Brown,et al.  Functional Biases in Visual Cortex Neurons with Identified Projections to Higher Cortical Targets , 2012, Current Biology.

[25]  J. Alonso,et al.  Complex Receptive Fields in Primary Visual Cortex , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[26]  P Redgrave,et al.  Movements resembling orientation or avoidance elicited by electrical stimulation of the superior colliculus in rats , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  Junichi Nakai,et al.  Comparison of genetically encoded calcium indicators for monitoring action potentials in mammalian brain by two-photon excitation fluorescence microscopy , 2015, Neurophotonics.

[28]  P. J. Sjöström,et al.  Functional specificity of local synaptic connections in neocortical networks , 2011, Nature.

[29]  C. Niell,et al.  Layer-Specific Refinement of Visual Cortex Function after Eye Opening in the Awake Mouse , 2015, The Journal of Neuroscience.

[30]  Martin Vinck,et al.  Arousal and Locomotion Make Distinct Contributions to Cortical Activity Patterns and Visual Encoding , 2014, Neuron.

[31]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[32]  Nicholas A. Steinmetz,et al.  Diverse coupling of neurons to populations in sensory cortex , 2015, Nature.

[33]  S. Hestrin,et al.  Intracortical circuits of pyramidal neurons reflect their long-range axonal targets , 2009, Nature.

[34]  D. Feldmeyer Excitatory neuronal connectivity in the barrel cortex , 2012, Front. Neuroanat..

[35]  D. Mumford,et al.  Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency , 2002, Nature Neuroscience.

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

[37]  G. Shepherd,et al.  The neocortical circuit: themes and variations , 2015, Nature Neuroscience.

[38]  R. Shapley,et al.  Orientation Selectivity in Macaque V1: Diversity and Laminar Dependence , 2002, The Journal of Neuroscience.

[39]  C. Petersen,et al.  The Excitatory Neuronal Network of the C2 Barrel Column in Mouse Primary Somatosensory Cortex , 2009, Neuron.

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

[41]  Allan R. Jones,et al.  A mesoscale connectome of the mouse brain , 2014, Nature.

[42]  Demetris K. Roumis,et al.  Functional Specialization of Mouse Higher Visual Cortical Areas , 2011, Neuron.

[43]  Michael J. Berry,et al.  Weak pairwise correlations imply strongly correlated network states in a neural population , 2005, Nature.

[44]  Sophia Rabe-Hesketh,et al.  Avoiding zero between‐study variance estimates in random‐effects meta‐analysis , 2013, Statistics in medicine.

[45]  HighWire Press The journal of neuroscience : the official journal of the Society for Neuroscience. , 1981 .

[46]  Scott T. Grafton,et al.  The striatum: where skills and habits meet. , 2015, Cold Spring Harbor perspectives in biology.

[47]  A L Pearlman,et al.  Laminar distribution of receptive field properties in the primary visual cortex of the mouse , 1980, The Journal of comparative neurology.

[48]  S. Mizumori,et al.  Role of the dorsomedial striatum in behavioral flexibility for response and visual cue discrimination learning. , 2002, Behavioral neuroscience.

[49]  Anthony J. Movshon,et al.  Visual Response Properties of Striate Cortical Neurons Projecting to Area MT in Macaque Monkeys , 1996, The Journal of Neuroscience.

[50]  Quanxin Wang,et al.  Stream-Related Preferences of Inputs to the Superior Colliculus from Areas of Dorsal and Ventral Streams of Mouse Visual Cortex , 2013, The Journal of Neuroscience.

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

[52]  Lindsey L. Glickfeld,et al.  Cortico-cortical projections in mouse visual cortex are functionally target specific , 2013, Nature Neuroscience.

[53]  C. Blakemore,et al.  Pyramidal neurons in layer 5 of the rat visual cortex. I. Correlation among cell morphology, intrinsic electrophysiological properties, and axon targets , 1994, The Journal of comparative neurology.

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

[55]  G. Shepherd Corticostriatal connectivity and its role in disease , 2013, Nature Reviews Neuroscience.