Long-Term Plasticity in Mouse Sensorimotor Circuits after Rhythmic Whisker Stimulation

Mice actively explore their environment by rhythmically sweeping their whiskers. As a consequence, neuronal activity in somatosensory pathways is modulated by the frequency of whisker movement. The potential role of rhythmic neuronal activity for the integration and consolidation of sensory signals, however, remains unexplored. Here, we show that a brief period of rhythmic whisker stimulation in anesthetized mice resulted in a frequency-specific long-lasting increase in the amplitude of somatosensory-evoked potentials in the contralateral primary somatosensory (barrel) cortex. Mapping of evoked potentials and intracortical recordings revealed that, in addition to potentiation in layers IV and II/III of the barrel cortex, rhythmic whisker stimulation induced a decrease of somatosensory-evoked responses in the supragranular layers of the motor cortex. To assess whether rhythmic sensory input-based plasticity might arise in natural settings, we exposed mice to environmental enrichment. We found that it resulted in somatosensory-evoked responses of increased amplitude, highlighting the influence of previous sensory experience in shaping sensory responses. Importantly, environmental enrichment-induced plasticity occluded further potentiation by rhythmic stimulation, indicating that both phenomena share common mechanisms. Overall, our results suggest that natural, rhythmic patterns of whisker activity can modify the cerebral processing of sensory information, providing a possible mechanism for learning during sensory perception.

[1]  Autumn L. Pruette,et al.  Sensory experience determines enrichment-induced plasticity in rat auditory cortex , 2007, Brain Research.

[2]  D. Lehmann,et al.  Principles of spatial analysis , 1987 .

[3]  M. Diamond,et al.  Rapid Fluctuations in Rat Barrel Cortex Plasticity , 2004, The Journal of Neuroscience.

[4]  M. Diamond,et al.  Neuronal Activity in Rat Barrel Cortex Underlying Texture Discrimination , 2007, PLoS biology.

[5]  T. J. Teyler,et al.  A method for calculating current source density (CSD) analysis without resorting to recording sites outside the sampling volume , 1988, Journal of Neuroscience Methods.

[6]  David Kleinfeld,et al.  Active sensation: insights from the rodent vibrissa sensorimotor system , 2006, Current Opinion in Neurobiology.

[7]  F. Ebner,et al.  Induction of high frequency activity in the somatosensory thalamus of rats in vivo results in long-term potentiation of responses in SI cortex , 2004, Experimental Brain Research.

[8]  Wickliffe C. Abraham,et al.  Rapid visual stimulation induces N-methyl-D-aspartate receptor-dependent sensory long-term potentiation in the rat cortex , 2006, Neuroreport.

[9]  D. Simons,et al.  Responses of rat trigeminal ganglion neurons to movements of vibrissae in different directions. , 1990, Somatosensory & motor research.

[10]  C Baumgartner,et al.  Laminar analysis of extracellular field potentials in rat vibrissa/barrel cortex. , 1990, Journal of neurophysiology.

[11]  B. Connors,et al.  Thalamocortical responses of mouse somatosensory (barrel) cortexin vitro , 1991, Neuroscience.

[12]  C. Petersen,et al.  Correlating whisker behavior with membrane potential in barrel cortex of awake mice , 2006, Nature Neuroscience.

[13]  D. Simons,et al.  Biometric analyses of vibrissal tactile discrimination in the rat , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Antoine Rémond,et al.  Methods of Analysis of Brain Electrical and Magnetic Signals , 1987 .

[15]  Alison L. Barth,et al.  Ongoing in Vivo Experience Triggers Synaptic Metaplasticity in the Neocortex , 2008, Science.

[16]  D. Barth,et al.  Topographic analysis of field potentials in rat vibrissa/barrel cortex , 1991, Brain Research.

[17]  Denis Brunet,et al.  Topographic ERP Analyses: A Step-by-Step Tutorial Review , 2008, Brain Topography.

[18]  M. Armstrong‐James,et al.  Flow of excitation within rat barrel cortex on striking a single vibrissa. , 1992, Journal of neurophysiology.

[19]  K. Fox,et al.  Is there a thalamic component to experience-dependent cortical plasticity? , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[20]  J. Lecas Locus coeruleus activation shortens synaptic drive while decreasing spike latency and jitter in sensorimotor cortex. Implications for neuronal integration , 2004, The European journal of neuroscience.

[21]  E. Ahissar,et al.  A neuronal analogue of state-dependent learning , 2000, Nature.

[22]  Shubhodeep Chakrabarti,et al.  Running Headline: Sensorimotor Integration in MI , 2022 .

[23]  A. Keller,et al.  Input-output organization of the rat vibrissal motor cortex , 2004, Experimental Brain Research.

[24]  C. Brunia,et al.  Sequential activation of microcircuits underlying somatosensory-evoked potentials in rat neocortex , 2004, Neuroscience.

[25]  T. Teyler,et al.  Induction of LTP in the human auditory cortex by sensory stimulation , 2005, The European journal of neuroscience.

[26]  U. Mitzdorf Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[27]  J. Donoghue,et al.  Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. , 1996, Journal of neurophysiology.

[28]  Daniel N. Hill,et al.  Texture Coding in the Rat Whisker System: Slip-Stick Versus Differential Resonance , 2008, PLoS biology.

[29]  David M Rector,et al.  Evoked response potential markers for anesthetic and behavioral states. , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

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

[31]  S. Czellár,et al.  Epicranial sensory evoked potential recordings for repeated assessment of cortical functions in mice , 2000, Journal of Neuroscience Methods.

[32]  D. Simons,et al.  Thalamocortical response transformation in the rat vibrissa/barrel system. , 1989, Journal of neurophysiology.

[33]  B. Sakmann,et al.  Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex , 2004, Nature.

[34]  Daniel J Simons,et al.  Response properties of whisker-associated trigeminothalamic neurons in rat nucleus principalis. , 2003, Journal of neurophysiology.

[35]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[36]  Mark F. Bear,et al.  Long-Term Potentiation of Thalamocortical Transmission in the Adult Visual Cortex In Vivo , 2001, The Journal of Neuroscience.

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

[38]  D Kleinfeld,et al.  Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. , 1997, Journal of neurophysiology.

[39]  C C Wood,et al.  Human cortical potentials evoked by stimulation of the median nerve. II. Cytoarchitectonic areas generating long-latency activity. , 1989, Journal of neurophysiology.

[40]  C E Schroeder,et al.  Neural generators of early cortical somatosensory evoked potentials in the awake monkey. , 1995, Electroencephalography and clinical neurophysiology.

[41]  C. Gilbert,et al.  The Neural Basis of Perceptual Learning , 2001, Neuron.

[42]  E. Welker,et al.  Recovery of evoked potentials, metabolic activity and behavior in a mouse model of somatosensory cortex lesion: role of the neural cell adhesion molecule (NCAM). , 2004, Cerebral cortex.

[43]  Blake W. Johnson,et al.  Long‐term potentiation of human visual evoked responses , 2005, The European journal of neuroscience.

[44]  J. Donoghue,et al.  Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  J. Donoghue,et al.  Learning-induced LTP in neocortex. , 2000, Science.

[46]  Christoph M. Michel,et al.  A mouse model for studying large-scale neuronal networks using EEG mapping techniques , 2008, NeuroImage.

[47]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[48]  C. C. Wood,et al.  Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating short-latency activity. , 1989, Journal of neurophysiology.

[49]  E. Welker,et al.  Modified sensory processing in the barrel cortex of the adult mouse after chronic whisker stimulation. , 2007, Journal of neurophysiology.