Motor Control by Sensory Cortex

By a Whisker Every student learns that the sensory cortex is used for processing sensation and the motor cortex is used for perceiving movement. However, in the real world, this may not always be so neatly arranged. Matyas et al. (p. 1240) have found that sensory and motor fields are specialized for different types of movement, such that in mice the motor cortex controlled the forward movement (protraction) of their whiskers and the sensory cortex controlled backwards movements (retraction) of whiskers. So if a whisker hits an object, then a reasonable first reaction might be a motor command for retraction. Similarly, the motor cortex stimulates protraction for more active exploration. Hence, the sensory cortex is also motor and the motor cortex is also sensory. In an ecological context, these combined reactions offer a repertoire useful for a mouse seeking food and shelter in a complex environment. Mouse whisker movements are controlled by both the sensory and motor cortex. Classical studies of mammalian movement control define a prominent role for the primary motor cortex. Investigating the mouse whisker system, we found an additional and equally direct pathway for cortical motor control driven by the primary somatosensory cortex. Whereas activity in primary motor cortex directly evokes exploratory whisker protraction, primary somatosensory cortex directly drives whisker retraction, providing a rapid negative feedback signal for sensorimotor integration. Motor control by sensory cortex suggests the need to reevaluate the functional organization of cortical maps.

[1]  D. Kleinfeld,et al.  'Where' and 'what' in the whisker sensorimotor system , 2008, Nature Reviews Neuroscience.

[2]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[3]  A. Keller,et al.  Functional circuitry involved in the regulation of whisker movements , 2002, The Journal of comparative neurology.

[4]  Michael Brecht,et al.  Whisker movements evoked by stimulation of single motor neurons in the facial nucleus of the rat. , 2008, Journal of neurophysiology.

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

[6]  C. Petersen,et al.  Long‐range connectivity of mouse primary somatosensory barrel cortex , 2010, The European journal of neuroscience.

[7]  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.

[8]  P. Strick,et al.  Muscle representation in the macaque motor cortex: an anatomical perspective. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[10]  T. Murphy,et al.  Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice , 2009, Nature Methods.

[11]  E. Bamberg,et al.  Channelrhodopsin-2, a directly light-gated cation-selective membrane channel , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  C. Petersen The Functional Organization of the Barrel Cortex , 2007, Neuron.

[13]  C. Woolsey,et al.  Motor effects of stimulation of cerebral cortex of squirrel monkey (Saimiri sciureus). , 1957, Journal of neurophysiology.

[14]  Benjamin R. Arenkiel,et al.  In Vivo Light-Induced Activation of Neural Circuitry in Transgenic Mice Expressing Channelrhodopsin-2 , 2007, Neuron.

[15]  K. Deisseroth,et al.  Millisecond-timescale, genetically targeted optical control of neural activity , 2005, Nature Neuroscience.

[16]  M. Graziano,et al.  Complex Movements Evoked by Microstimulation of Precentral Cortex , 2002, Neuron.

[17]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[18]  R. Reid,et al.  Direct Activation of Sparse, Distributed Populations of Cortical Neurons by Electrical Microstimulation , 2009, Neuron.

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

[20]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[21]  Tomoki Fukai,et al.  Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements , 2009, Nature Neuroscience.

[22]  Michael Brecht,et al.  Barrel cortex and whisker-mediated behaviors , 2007, Current Opinion in Neurobiology.

[23]  Jerald D. Kralik,et al.  Real-time prediction of hand trajectory by ensembles of cortical neurons in primates , 2000, Nature.

[24]  S. Wise,et al.  The motor cortex of the rat: Cytoarchitecture and microstimulation mapping , 1982, The Journal of comparative neurology.

[25]  E. G. Jones,et al.  Differential distribution of corticospinal projections from individual cytoarchitectonic fields in the monkey , 1977, Brain Research.

[26]  D. Tank,et al.  Functional Clustering of Neurons in Motor Cortex Determined by Cellular Resolution Imaging in Awake Behaving Mice , 2009, The Journal of Neuroscience.

[27]  P. Buisseret,et al.  Trigeminal projections to hypoglossal and facial motor nuclei in the rat , 1999, The Journal of comparative neurology.

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

[29]  E. Seidemann,et al.  Dynamics of Depolarization and Hyperpolarization in the Frontal Cortex and Saccade Goal , 2002, Science.

[30]  M. Jacquin,et al.  Structure-function relationships in rat brain stem subnucleus interpolaris. VIII. Cortical inputs. , 1990, Journal of neurophysiology.

[31]  Cornelius Schwarz,et al.  Spatial Segregation of Different Modes of Movement Control in the Whisker Representation of Rat Primary Motor Cortex , 2005, The Journal of Neuroscience.

[32]  Nicholas G. Hatsopoulos,et al.  Brain-machine interface: Instant neural control of a movement signal , 2002, Nature.