Activity in motor-sensory projections reveals distributed coding in somatosensation

Cortical-feedback projections to primary sensory areas terminate most heavily in layer 1 (L1) of the neocortex , where they make synapses with tuft dendrites of pyramidal neurons. L1 input is thought to provide ‘contextual’ information, but the signals transmitted by L1 feedback remain uncharacterized. In the rodent somatosensory system, the spatially diffuse feedback projection from vibrissal motor cortex (vM1) to vibrissal somatosensory cortex (vS1, also known as the barrel cortex) may allow whisker touch to be interpreted in the context of whisker position to compute object location. When mice palpate objects with their whiskers to localize object features, whisker touch excites vS1 and later vM1 in a somatotopic manner. Here we use axonal calcium imaging to track activity in vM1→vS1 afferents in L1 of the barrel cortex while mice performed whisker-dependent object localization. Spatially intermingled individual axons represent whisker movements, touch and other behavioural features. In a subpopulation of axons, activity depends on object location and persists for seconds after touch. Neurons in the barrel cortex thus have information to integrate movements and touches of multiple whiskers over time, key components of object identification and navigation by active touch.

[1]  Jochen F Staiger,et al.  Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex , 2012, Nature Neuroscience.

[2]  Trevor Hastie,et al.  The Elements of Statistical Learning , 2001 .

[3]  Per Magne Knutsen,et al.  Orthogonal coding of object location , 2009, Trends in Neurosciences.

[4]  Vijay Iyer,et al.  Ephus: Multipurpose Data Acquisition Software for Neuroscience Experiments , 2010, Front. Neural Circuits.

[5]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[6]  Michael P Stryker,et al.  TrkB kinase is required for recovery, but not loss, of cortical responses following monocular deprivation , 2008, Nature Neuroscience.

[7]  Bryan M. Hooks,et al.  Laminar Analysis of Excitatory Local Circuits in Vibrissal Motor and Sensory Cortical Areas , 2011, PLoS biology.

[8]  J. Krakauer,et al.  Error correction, sensory prediction, and adaptation in motor control. , 2010, Annual review of neuroscience.

[9]  W. Senn,et al.  Top-down dendritic input increases the gain of layer 5 pyramidal neurons. , 2004, Cerebral cortex.

[10]  Martin Deschênes,et al.  Single‐cell study of motor cortex projections to the barrel field in rats , 2003, The Journal of comparative neurology.

[11]  B. Sakmann,et al.  Calcium dynamics associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex , 2000, The Journal of physiology.

[12]  Rafael Yuste,et al.  Fast nonnegative deconvolution for spike train inference from population calcium imaging. , 2009, Journal of neurophysiology.

[13]  Leo Breiman,et al.  Random Forests , 2001, Machine Learning.

[14]  M. Brecht,et al.  Tactile guidance of prey capture in Etruscan shrews , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[15]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[16]  D. Tank,et al.  Action potentials reliably invade axonal arbors of rat neocortical neurons. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Daniel N. Hill,et al.  Primary Motor Cortex Reports Efferent Control of Vibrissa Motion on Multiple Timescales , 2011, Neuron.

[18]  G. Stuart,et al.  Dependence of EPSP Efficacy on Synapse Location in Neocortical Pyramidal Neurons , 2002, Science.

[19]  Karel Svoboda,et al.  Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice , 2010, Nature.

[20]  L. Cauller,et al.  Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[22]  Nathalie L Rochefort,et al.  Functional mapping of single spines in cortical neurons in vivo , 2011, Nature.

[23]  Bert Sakmann,et al.  Dendritic coding of multiple sensory inputs in single cortical neurons in vivo , 2011, Proceedings of the National Academy of Sciences.

[24]  Daniel N. Hill,et al.  Biomechanics of the Vibrissa Motor Plant in Rat: Rhythmic Whisking Consists of Triphasic Neuromuscular Activity , 2008, The Journal of Neuroscience.

[25]  Nathan G. Clack,et al.  Vibrissa-Based Object Localization in Head-Fixed Mice , 2010, The Journal of Neuroscience.

[26]  K. Svoboda,et al.  Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex , 2002, Nature.

[27]  D. Margoliash,et al.  Song replay during sleep and computational rules for sensorimotor vocal learning. , 2000, Science.

[28]  M. Nicolelis,et al.  Behavioral Properties of the Trigeminal Somatosensory System in Rats Performing Whisker-Dependent Tactile Discriminations , 2001, The Journal of Neuroscience.

[29]  R D Frostig,et al.  Characterization of functional organization within rat barrel cortex using intrinsic signal optical imaging through a thinned skull. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Erkki Oja,et al.  Independent component analysis: algorithms and applications , 2000, Neural Networks.

[31]  Eugene W. Myers,et al.  Automated Tracking of Whiskers in Videos of Head Fixed Rodents , 2012, PLoS Comput. Biol..

[32]  B W Connors,et al.  Backward cortical projections to primary somatosensory cortex in rats extend long horizontal axons in layer I , 1998, The Journal of comparative neurology.

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

[34]  K. Svoboda,et al.  Cell Type-Specific Structural Plasticity of Axonal Branches and Boutons in the Adult Neocortex , 2006, Neuron.

[35]  Stephen R. Williams,et al.  Encoding and Decoding of Dendritic Excitation during Active States in Pyramidal Neurons , 2022 .

[36]  D. Tank,et al.  In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons , 1999, Nature Neuroscience.

[37]  B. Sakmann,et al.  Spiking in primary somatosensory cortex during natural whisking in awake head-restrained rats is cell-type specific , 2009, Proceedings of the National Academy of Sciences.

[38]  B. Sakmann,et al.  A new cellular mechanism for coupling inputs arriving at different cortical layers , 1999, Nature.

[39]  Nathalie L Rochefort,et al.  Dendritic organization of sensory input to cortical neurons in vivo , 2010, Nature.

[40]  D. Kleinfeld,et al.  Phase-to-rate transformations encode touch in cortical neurons of a scanning sensorimotor system , 2009, Nature Neuroscience.

[41]  W. Senn,et al.  Dendritic encoding of sensory stimuli controlled by deep cortical interneurons , 2009, Nature.

[42]  L. Cauller Layer I of primary sensory neocortex: where top-down converges upon bottom-up , 1995, Behavioural Brain Research.

[43]  D. Kleinfeld,et al.  Adaptive Filtering of Vibrissa Input in Motor Cortex of Rat , 2002, Neuron.

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

[45]  Joseph H. Solomon,et al.  Biomechanical models for radial distance determination by the rat vibrissal system. , 2007, Journal of neurophysiology.

[46]  P W Davidson,et al.  Haptic judgments of curvature by blind and sighted humans. , 1972, Journal of experimental psychology.

[47]  Eugene W. Myers,et al.  Automated Reconstruction of Neuronal Morphology Based on Local Geometrical and Global Structural Models , 2011, Neuroinformatics.

[48]  A. Polsky,et al.  Synaptic Integration in Tuft Dendrites of Layer 5 Pyramidal Neurons: A New Unifying Principle , 2009, Science.

[49]  Per Magne Knutsen,et al.  Haptic Object Localization in the Vibrissal System: Behavior and Performance , 2006, The Journal of Neuroscience.

[50]  David G. Stork,et al.  Pattern Classification , 1973 .

[51]  E G Jones,et al.  Inhibitory synaptogenesis in mouse somatosensory cortex. , 1997, Cerebral cortex.

[52]  D J Simons,et al.  The relationship of vibrissal motor cortex unit activity to whisking in the awake rat. , 1996, Somatosensory & motor research.

[53]  David S. Greenberg,et al.  Automated correction of fast motion artifacts for two-photon imaging of awake animals , 2009, Journal of Neuroscience Methods.

[54]  Karel Svoboda,et al.  Long-Range Neuronal Circuits Underlying the Interaction between Sensory and Motor Cortex , 2011, Neuron.

[55]  Mark J. Schnitzer,et al.  Automated Analysis of Cellular Signals from Large-Scale Calcium Imaging Data , 2009, Neuron.

[56]  K. Svoboda,et al.  Neural Activity in Barrel Cortex Underlying Vibrissa-Based Object Localization in Mice , 2010, Neuron.

[57]  K. Svoboda,et al.  The subcellular organization of neocortical excitatory connections , 2009, Nature.

[58]  D Kleinfeld,et al.  Anatomical loops and their electrical dynamics in relation to whisking by rat. , 1999, Somatosensory & motor research.

[59]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

[60]  Erik Seedhouse,et al.  Behavior and performance , 2011 .

[61]  N. Spruston Pyramidal neurons: dendritic structure and synaptic integration , 2008, Nature Reviews Neuroscience.

[62]  R. Wurtz,et al.  Brain circuits for the internal monitoring of movements. , 2008, Annual review of neuroscience.

[63]  F. Haiss,et al.  Spatiotemporal Dynamics of Cortical Sensorimotor Integration in Behaving Mice , 2007, Neuron.

[64]  J. Magee,et al.  Pathway Interactions and Synaptic Plasticity in the Dendritic Tuft Regions of CA1 Pyramidal Neurons , 2009, Neuron.

[65]  B. Sakmann,et al.  Unsupervised whisker tracking in unrestrained behaving animals. , 2008, Journal of neurophysiology.

[66]  Sreekanth H. Chalasani,et al.  Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators , 2009, Nature Methods.

[67]  Manuel Guizar-Sicairos,et al.  Efficient subpixel image registration algorithms. , 2008, Optics letters.