Rat whisker motor cortex is subdivided into sensory-input and motor-output areas

Rodent whisking is an exploratory behavior that can be modified by sensory feedback. Consistent with this, many whisker-sensitive cortical regions project to agranular motor [motor cortex (MI)] cortex, but the relative topography of these afferent projections has not been established. Intracortical microstimulation (ICMS) evokes whisker movements that are used to map the functional organization of MI, but no study has compared the whisker-related inputs to MI with the ICMS sites that evoke whisker movements. To elucidate this relationship, anterograde tracers were placed in posterior parietal cortex (PPC) and in the primary somatosensory (SI) and secondary somatosensory (SII) cortical areas so that their labeled projections to MI could be analyzed with respect to ICMS sites that evoke whisker movements. Projections from SI and SII terminate in a narrow zone that marks the transition between the medial agranular (AGm) and lateral agranular (AGl) cortical areas, but PPC projects more medially and terminates in AGm proper. Paired recordings of MI neurons indicate that the region between AGm and AGl is highly responsive to whisker deflections, but neurons in AGm display negligible responses to whisker stimulation. By contrast, AGm microstimulation is more effective in evoking whisker movements than microstimulation of the transitional region between AGm and AGl. The AGm region was also found to contain a larger concentration of corticotectal neurons, which could convey whisker-related information to the facial nucleus. These results indicate that rat whisker MI is comprised of at least two functionally distinct subregions: a sensory processing zone in the transitional region between AGm and AGl, and a motor-output region located more medially in AGm proper.

[1]  F. Ebner,et al.  Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. , 1999, Journal of neurophysiology.

[2]  W. Welker Analysis of Sniffing of the Albino Rat 1) , 1964 .

[3]  John H. Martin,et al.  The Transition from Development to Motor Control Function in the Corticospinal System , 2004, The Journal of Neuroscience.

[4]  Kevin D Alloway,et al.  Information processing streams in rodent barrel cortex: the differential functions of barrel and septal circuits. , 2008, Cerebral cortex.

[5]  U. Kim,et al.  Interconnected cortical networks between primary somatosensory cortex septal columns and posterior parietal cortex in rat , 2011, The Journal of comparative neurology.

[6]  Niranjan A. Kambi,et al.  Overlapping representations of the neck and whiskers in the rat motor cortex revealed by mapping at different anaesthetic depths , 2007, The European journal of neuroscience.

[7]  Asaf Keller,et al.  Superior colliculus control of vibrissa movements. , 2008, Journal of neurophysiology.

[8]  Jeffrey C. Erlich,et al.  A Cortical Substrate for Memory-Guided Orienting in the Rat , 2011, Neuron.

[9]  J. Kaas,et al.  Microelectrode maps, myeloarchitecture, and cortical connections of three somatotopically organized representations of the body surface in the parietal cortex of squirrels , 1986, The Journal of comparative neurology.

[10]  A Keller,et al.  Specific patterns of intrinsic connections between representation zones in the rat motor cortex. , 1994, Cerebral cortex.

[11]  Kevin D. Alloway,et al.  Differential topography of the bilateral cortical projections to the whisker and forepaw regions in rat motor cortex , 2009, Brain Structure and Function.

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

[13]  C. Wilson,et al.  Corticostriatal innervation of the patch and matrix in the rat neostriatum , 1996, The Journal of comparative neurology.

[14]  Nathan P Cramer,et al.  Cortical control of a whisking central pattern generator. , 2006, Journal of neurophysiology.

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

[16]  M. Wong-Riley Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

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

[18]  Mara Fabri,et al.  Ipsilateral cortical connections of primary somatic sensory cortex in rats , 1991, The Journal of comparative neurology.

[19]  Michael Brecht,et al.  Organization of rat vibrissa motor cortex and adjacent areas according to cytoarchitectonics, microstimulation, and intracellular stimulation of identified cells , 2004, The Journal of comparative neurology.

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

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

[22]  Shubhodeep Chakrabarti,et al.  Differential origin of projections from SI barrel cortex to the whisker representations in SII and MI , 2006, The Journal of comparative neurology.

[23]  Barry E. Stein,et al.  Eye movements evoked by electrical stimulation in the superior colliculus of rats and hamsters , 1982, Brain Research.

[24]  David Kleinfeld,et al.  Vibrissa movement elicited by rhythmic electrical microstimulation to motor cortex in the aroused rat mimics exploratory whisking. , 2003, Journal of neurophysiology.

[25]  R. Reep,et al.  Topographic organization in the corticocortical connections of medial agranular cortex in rats , 1990, The Journal of comparative neurology.

[26]  K. Alloway,et al.  Thalamic POm projections to the dorsolateral striatum of rats: potential pathway for mediating stimulus-response associations for sensorimotor habits. , 2012, Journal of neurophysiology.

[27]  K. Alloway,et al.  Septal columns in rodent barrel cortex: Functional circuits for modulating whisking behavior , 2004, The Journal of comparative neurology.

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

[29]  J. Hoover,et al.  Sensorimotor corticocortical projections from rat barrel cortex have an anisotropic organization that facilitates integration of inputs from whiskers in the same row , 2003, The Journal of comparative neurology.

[30]  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.

[31]  Kevin D Alloway,et al.  Functional circuits mediating sensorimotor integration: Quantitative comparisons of projections from rodent barrel cortex to primary motor cortex, neostriatum, superior colliculus, and the pons , 2005, The Journal of comparative neurology.

[32]  M. Brecht,et al.  Monosynaptic Pathway from Rat Vibrissa Motor Cortex to Facial Motor Neurons Revealed by Lentivirus-Based Axonal Tracing , 2005, The Journal of Neuroscience.

[33]  R. Reep,et al.  Posterior parietal cortex as part of a neural network for directed attention in rats , 2009, Neurobiology of Learning and Memory.

[34]  J. Kleim,et al.  The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. , 2011, Cerebral cortex.

[35]  G. Quirk,et al.  The organization of the rat motor cortex: A microstimulation mapping study , 1986, Brain Research Reviews.

[36]  J. Olavarria,et al.  Areal and laminar organization of corticocortical projections in the rat somatosensory cortex , 1990, The Journal of comparative neurology.

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

[38]  K. Alloway,et al.  Quantitative analysis of the bilateral brainstem projections from the whisker and forepaw regions in rat primary motor cortex , 2010, The Journal of comparative neurology.

[39]  D. Simons,et al.  Cytochrome oxidase staining in the rat smI barrel cortex , 1985, The Journal of comparative neurology.

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

[41]  K. Sanderson,et al.  Reevaluation of motor cortex and of sensorimotor overlap in cerebral cortex of albino rats , 1984, Brain Research.

[42]  R. Reep,et al.  Disconnection of medial agranular and posterior parietal cortex produces multimodal neglect in rats , 1997, Behavioural Brain Research.

[43]  Asaf Keller,et al.  Superior sensation: superior colliculus participation in rat vibrissa system. , 2007 .

[44]  T. Voigt,et al.  Synaptophysin immunohistochemistry reveals inside‐out pattern of early synaptogenesis in ferret cerebral cortex , 1993, The Journal of comparative neurology.

[45]  R. Hall,et al.  Organization of motor and somatosensory neocortex in the albino rat , 1974 .