Functional circuits mediating sensorimotor integration: Quantitative comparisons of projections from rodent barrel cortex to primary motor cortex, neostriatum, superior colliculus, and the pons

Motor performance depends on somatosensory feedback, and consistent with this finding, primary somatosensory (SI) cortex projects to several regions involved in motor control. Although the pathways mediating sensorimotor integration are known, few studies have compared their projection patterns. Therefore, in each animal, we injected two anterograde tracers into SI barrel cortex and compared the relative density and spatial extent of the labeled projections to the primary motor (MI) cortex, neostriatum, superior colliculus, and basal pons. Quantitative analysis revealed that these projections terminated most extensively in the neostriatum, to a lesser extent in MI cortex, and innervated the least amount of neuropil in the superior colliculus and pontine nuclei. Tracer overlap in the pontine nuclei was significantly higher than in the other three brains regions, and was strongly correlated with overlap in the superior colliculus, presumably because some projections to these two brain regions represent collaterals of the same neurons. The density of labeled varicosities was highest in the pons and lowest in MI. As a proportion of total labeling, densely packed clusters of labeled terminals were most prevalent in the pons, less prevalent in neostriatum and superior colliculus, and least prevalent in MI cortex. These results are consistent with physiological evidence indicating strong coherence between SI barrel cortex and the cerebellum during whisking behavior. J. Comp. Neurol. 488:82–100, 2005. © 2005 Wiley‐Liss, Inc.

[1]  J. Deniau,et al.  Synaptic Convergence of Motor and Somatosensory Cortical Afferents onto GABAergic Interneurons in the Rat Striatum , 2002, The Journal of Neuroscience.

[2]  S. Mori,et al.  The superior colliculus relays signals descending from the vibrissal motor cortex to the facial nerve nucleus in the rat , 1995, Neuroscience Letters.

[3]  C. Watt,et al.  Projections to the basilar pontine nuclei from face sensory and motor regions of the cerebral cortex in the rat , 1985, The Journal of comparative neurology.

[4]  M. L. Pucak,et al.  Dendritic morphology of callosal and ipsilateral projection neurons in monkey prefrontal cortex , 2002, Neuroscience.

[5]  G. Arbuthnott,et al.  Identification of the source of the bilateral projection system from cortex to somatosensory neostriatum and an exploration of its physiological actions , 2001, Neuroscience.

[6]  Kevin D. Alloway,et al.  Quantitative comparisons of corticothalamic topography within the ventrobasal complex and the posterior nucleus of the rodent thalamus , 2003, Brain Research.

[7]  J M Bower,et al.  Principles of organization of a cerebro-cerebellar circuit. Micromapping the projections from cerebral (SI) to cerebellar (granule cell layer) tactile areas of rats. , 1981, Brain, behavior and evolution.

[8]  J M Bower,et al.  Control of sensory data acquisition. , 1997, International review of neurobiology.

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

[10]  Charles J. Wilson,et al.  Corticostriatal combinatorics: the implications of corticostriatal axonal arborizations. , 2002, Journal of neurophysiology.

[11]  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.

[12]  T. Leergaard,et al.  Three‐dimensional topography of corticopontine projections from rat sensorimotor cortex: Comparisons with corticostriatal projections reveal diverse integrative organization , 2004, The Journal of comparative neurology.

[13]  J. Bower,et al.  Contribution of somatosensory cortex to responses in the rat cerebellar granule cell layer following peripheral tactile stimulation , 1996, Experimental Brain Research.

[14]  J. Hoover,et al.  Projections from primary somatosensory cortex to the neostriatum: the role of somatotopic continuity in corticostriatal convergence. , 2003, Journal of neurophysiology.

[15]  H. Killackey,et al.  Trigeminal projections to the superior colliculus of the rat , 1981, The Journal of comparative neurology.

[16]  L. Brown,et al.  Organizing principles of cortical integration in the rat neostriatum: Corticostriate map of the body surface is an ordered lattice of curved laminae and radial points , 1998, The Journal of comparative neurology.

[17]  T. Leergaard,et al.  Three-Dimensional Topography of Corticopontine Projections from Rat Barrel Cortex: Correlations with Corticostriatal Organization , 2000, The Journal of Neuroscience.

[18]  David Kleinfeld,et al.  Closed-loop neuronal computations: focus on vibrissa somatosensation in rat. , 2003, Cerebral cortex.

[19]  Anna Devor,et al.  In vivo tracing of major rat brain pathways using manganese-enhanced magnetic resonance imaging and three-dimensional digital atlasing , 2003, NeuroImage.

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

[21]  J G Bjaalie,et al.  Salient anatomic features of the cortico-ponto-cerebellar pathway. , 1997, Progress in brain research.

[22]  K. J. Cole,et al.  Sensory-motor coordination during grasping and manipulative actions , 1992, Current Biology.

[23]  K. Alloway,et al.  Organization of corticostriatal projections from the vibrissal representations in the primary motor and somatosensory cortical areas of rodents , 2001, The Journal of comparative neurology.

[24]  J. Bower,et al.  Rat somatosensory cerebropontocerebellar pathways: Spatial relationships of the somatotopic map of the primary somatosensory cortex are preserved in a three‐dimensional clustered pontine map , 2000, The Journal of comparative neurology.

[25]  C. Wilson,et al.  Intracellular recording of identified neostriatal patch and matrix spiny cells in a slice preparation preserving cortical inputs. , 1989, Journal of neurophysiology.

[26]  H. Kuypers,et al.  Branching cortical neurons in cat which project to the colliculi and to the pons: a retrograde fluorescent double-labeling study , 2004, Experimental Brain Research.

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

[28]  M. Deschenes,et al.  Axonal arborizations of corticostriatal and corticothalamic fibers arising from the second somatosensory area in the rat. , 1996, Cerebral cortex.

[29]  S. Wise,et al.  Somatotopic and columnar organization in the corticotectal projection of the rat somatic sensory cortex , 1977, Brain Research.

[30]  R. Izraeli,et al.  Vibrissal motor cortex in the rat: connections with the barrel field , 2004, Experimental Brain Research.

[31]  C. Wilson,et al.  Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  L. Brown Somatotopic organization in rat striatum: evidence for a combinational map. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Trygve B. Leergaard,et al.  Topographical organization in the early postnatal projection: A carbocyanine dye and 3‐D computer reconstruction study in the rat , 1995 .

[34]  R. Malach,et al.  Mosaic architecture of the somatic sensory-recipient sector of the cat's striatum , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  M. West,et al.  Representation of the body by single neurons in the dorsolateral striatum of the awake, unrestrained rat , 1991, The Journal of comparative neurology.

[36]  J. Donoghue,et al.  Afferent connections of the lateral agranular field of the rat motor cortex , 1983, The Journal of comparative neurology.

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

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

[39]  J. Tigges,et al.  Efferents of area 4 in a South American monkey (Saimiri) I. Terminations in the spinal cord , 1979, Brain Research.

[40]  K. Berridge,et al.  Implementation of Action Sequences by a Neostriatal Site: A Lesion Mapping Study of Grooming Syntax , 1996, The Journal of Neuroscience.

[41]  M. Deschenes,et al.  Corticostriatal projections from layer V cells in rat are collaterals of long-range corticofugal axons , 1996, Brain Research.

[42]  M. Wiesendanger,et al.  Corticomotoneuronal connections in the rat: Evidence from double‐labeling of motoneurons and corticospinal axon arborizations , 1991, The Journal of comparative neurology.

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

[44]  S. Wise,et al.  Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex , 1977, The Journal of comparative neurology.

[45]  A. Graybiel,et al.  Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body-part representations. , 1991, Journal of neurophysiology.

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

[47]  J G Bjaalie,et al.  Topographical organization in the early postnatal corticopontine projection: a carbocyanine dye and 3-D computer reconstruction study in the rat. , 1995, The Journal of comparative neurology.

[48]  J. W. Aldridge,et al.  Coding of Serial Order by Neostriatal Neurons: A “Natural Action” Approach to Movement Sequence , 1998, The Journal of Neuroscience.

[49]  M. Glickstein,et al.  Whiskers, barrels, and cortical efferent pathways in gap crossing by rats. , 2000, Journal of neurophysiology.

[50]  Verne S. Caviness,et al.  Somata of layer V projection neurons in the mouse barrelfield cortex are in preferential register with the sides and septa of the barrels , 1986, Neuroscience Letters.

[51]  Charles J. Wilson,et al.  Connectivity and Convergence of Single Corticostriatal Axons , 1998, The Journal of Neuroscience.

[52]  Subcortical projections of the parietal lobes. , 2003, Advances in neurology.

[53]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

[54]  S. T. Kitai,et al.  Medium spiny neuron projection from the rat striatum: An intracellular horseradish peroxidase study , 1980, Brain Research.

[55]  J. Chapin,et al.  Mapping the body representation in the SI cortex of anesthetized and awake rats , 1984, The Journal of comparative neurology.

[56]  D. Buxton,et al.  Origins and collateralization of corticospinal, corticopontine, corticorubral and corticostriatal tracts: a multiple retrograde fluorescent tracing study , 1992, Brain Research.

[57]  G. Mower,et al.  Cat visual corticopontine cells project to the superior colliculus , 1983, Brain Research.

[58]  J. Jacobs,et al.  Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. , 2001, Cerebral cortex.

[59]  R. North,et al.  Membrane properties and synaptic responses of rat striatal neurones in vitro. , 1991, The Journal of physiology.

[60]  H P Zeigler,et al.  Cortical barrel field ablation and unconditioned whisking kinematics , 2001, Somatosensory & motor research.

[61]  J. Bower,et al.  Cerebellum Implicated in Sensory Acquisition and Discrimination Rather Than Motor Control , 1996, Science.

[62]  G. Arbuthnott,et al.  Double anterograde tracing of outputs from adjacent “barrel columns” of rat somatosensory cortex. Neostriatal projection patterns and terminal ultrastructure , 1999, Neuroscience.

[63]  J. Kassel Somatotopic organization of SI corticotectal projections in rats , 1982, Brain Research.

[64]  J. Hoover,et al.  Divergent corticostriatal projections from a single cortical column in the somatosensory cortex of rats , 1998, Brain Research.

[65]  Somatosensory input onto pyramidal tract neurons in rodent motor cortex. , 1996, Neuroreport.

[66]  Charles J. Wilson,et al.  Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: A study employing intracellular injection of horseradish peroxidase , 1980 .

[67]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

[68]  B. Schofield,et al.  Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurons in layer V of primary visual cortex of the hooded rat , 1988, The Journal of comparative neurology.

[69]  D. Pandya,et al.  The cerebrocerebellar system. , 1997, International review of neurobiology.

[70]  Roland S Johansson,et al.  Dynamic use of tactile afferent signals in control of dexterous manipulation. , 2002, Advances in experimental medicine and biology.

[71]  J. Hoover,et al.  Overlapping corticostriatal projections from the rodent vibrissal representations in primary and secondary somatosensory cortex. , 2000, The Journal of comparative neurology.

[72]  A. Flaherty,et al.  Input-output organization of the sensorimotor striatum in the squirrel monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[73]  P. Thier,et al.  Modular organization of the pontine nuclei: dendritic fields of identified pontine projection neurons in the rat respect the borders of cortical afferent fields , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[74]  J Xiong,et al.  Lateral cerebellar hemispheres actively support sensory acquisition and discrimination rather than motor control. , 1997, Learning & memory.

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

[76]  M. Aoki,et al.  Tracing of corticospinal fibers by extracellular pressure-injection of biocytin into the motor cortex in rats , 1993, Neuroscience Research.

[77]  D. Kleinfeld,et al.  Coherent electrical activity between vibrissa sensory areas of cerebellum and neocortex is enhanced during free whisking. , 2002, Journal of neurophysiology.

[78]  M Glickstein,et al.  Basal ganglia and cerebellum receive different somatosensory information in rats. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[79]  David Kleinfeld,et al.  Current flow in vibrissa motor cortex can phase-lock with exploratory rhythmic whisking in rat. , 2004, Journal of neurophysiology.

[80]  M. Wiesendanger,et al.  The corticopontine system in the rat. II. The projection pattern , 1982, The Journal of comparative neurology.

[81]  K. Alloway,et al.  Corticostriatal Projections from Rat Barrel Cortex Have an Anisotropic Organization that Correlates with Vibrissal Whisking Behavior , 1999, The Journal of Neuroscience.