Integration of sensory and motor representations of single fingers in the human cerebellum.

The cerebellum is thought to play a key role in the integration of sensory and motor events. Little is known, however, about how sensory and motor maps in the cerebellum superimpose. In the present study we investigated the relationship between these two maps for the representation of single fingers. Participants made isometric key presses with individual fingers or received vibratory tactile stimulation to the fingertips while undergoing high-resolution functional magnetic resonance imaging (fMRI). Using multivariate analysis, we have demonstrated that the ipsilateral lobule V and VIII show patterns of activity that encode, within the same region, both which finger pressed and which finger was stimulated. The individual finger-specific activation patches are smaller than 3 mm and only show a weak somatotopic organization. To study the superposition of sensory and motor maps, we correlated the finger-specific patterns across the two conditions. In the neocortex, sensory stimulation of one digit led to activation of the same patches as force production by the same digit; in the cerebellum, these activation patches were organized in an uncorrelated manner. This suggests that, in the cerebellum, a movement of a particular finger is paired with a range of possible sensory outcomes. In summary, our results indicate a small and fractured representation of single digits in the cerebellum and suggest a fundamental difference in how the cerebellum and the neocortex integrate sensory and motor events.

[1]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[2]  M. Erb,et al.  Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization , 2001, Human brain mapping.

[3]  Yasmin L. Hashambhoy,et al.  Neural Correlates of Reach Errors , 2005, The Journal of Neuroscience.

[4]  Michael Erb,et al.  From will to action: sequential cerebellar contributions to voluntary movement , 2003, NeuroImage.

[5]  Tom M. Mitchell,et al.  Machine learning classifiers and fMRI: A tutorial overview , 2009, NeuroImage.

[6]  M. Garwicz,et al.  Anatomical and physiological foundations of cerebellar information processing , 2005, Nature Reviews Neuroscience.

[7]  John E. Schlerf,et al.  Evidence of a novel somatopic map in the human neocerebellum during complex actions. , 2010, Journal of neurophysiology.

[8]  Gary W Thickbroom,et al.  Dual representation of the hand in the cerebellum: activation with voluntary and passive finger movement , 2003, NeuroImage.

[9]  Robert Chen,et al.  Digit somatotopy within cortical areas of the postcentral gyrus in humans. , 2008, Cerebral cortex.

[10]  P. Boesiger,et al.  SENSE: Sensitivity encoding for fast MRI , 1999, Magnetic resonance in medicine.

[11]  R. Ivry,et al.  Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. , 2005, Journal of neurophysiology.

[12]  M. Schieber,et al.  How somatotopic is the motor cortex hand area? , 1993, Science.

[13]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[14]  R. Savoy Functional Magnetic Resonance Imaging (fMRI) , 2002 .

[15]  J. Gallant,et al.  Identifying natural images from human brain activity , 2008, Nature.

[16]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[17]  Alexander Borst,et al.  How does Nature Program Neuron Types? , 2008, Front. Neurosci..

[18]  J. Perlmutter,et al.  Vibration-Induced Regional Cerebral Blood Flow Responses in Normal Aging , 1992, Journal of Cerebral Blood Flow and Metabolism.

[19]  J. Desmond,et al.  Lobular Patterns of Cerebellar Activation in Verbal Working-Memory and Finger-Tapping Tasks as Revealed by Functional MRI , 1997, The Journal of Neuroscience.

[20]  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.

[21]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[22]  Yi Zhang,et al.  Attenuation of activity-induced increases in cerebellar blood flow by lesion of the inferior olive. , 2003, American journal of physiology. Heart and circulatory physiology.

[23]  Marc H Schieber,et al.  Motor cortex and the distributed anatomy of finger movements. , 2002, Advances in experimental medicine and biology.

[24]  C. Woolsey,et al.  Localization in somatic sensory and motor areas of human cerebral cortex as determined by direct recording of evoked potentials and electrical stimulation. , 1979, Journal of neurosurgery.

[25]  D. Attwell,et al.  The neural basis of functional brain imaging signals , 2002, Trends in Neurosciences.

[26]  Jörn Diedrichsen,et al.  Advances in functional imaging of the human cerebellum. , 2010, Current opinion in neurology.

[27]  A. Schleicher,et al.  Integration of microstructural and functional aspects of human somatosensory areas 3a, 3b, and 1 on the basis of a computerized brain atlas , 2001, Anatomy and Embryology.

[28]  N Ramnani,et al.  A probabilistic MR atlas of the human cerebellum , 2009, NeuroImage.

[29]  G. Rees,et al.  Predicting the Stream of Consciousness from Activity in Human Visual Cortex , 2005, Current Biology.

[30]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

[31]  D. Wolpert,et al.  Internal models in the cerebellum , 1998, Trends in Cognitive Sciences.

[32]  A. Bastian Learning to predict the future: the cerebellum adapts feedforward movement control , 2006, Current Opinion in Neurobiology.

[33]  Jascha D. Swisher,et al.  Multiscale Pattern Analysis of Orientation-Selective Activity in the Primary Visual Cortex , 2010, The Journal of Neuroscience.

[34]  R. Shadmehr,et al.  Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration. , 2005, Journal of neurophysiology.

[35]  Nikolaus Kriegeskorte,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[36]  W. T. Thach,et al.  Functional mapping of the human cerebellum with positron emission tomography. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[37]  N. Kriegeskorte,et al.  Revealing representational content with pattern-information fMRI--an introductory guide. , 2009, Social cognitive and affective neuroscience.

[38]  Nikolaus Kriegeskorte,et al.  Comparison of multivariate classifiers and response normalizations for pattern-information fMRI , 2010, NeuroImage.

[39]  Guy Marchal,et al.  Automated multi-moda lity image registration based on information theory , 1995 .

[40]  P. Strick,et al.  Cerebellar Loops with Motor Cortex and Prefrontal Cortex of a Nonhuman Primate , 2003, The Journal of Neuroscience.

[41]  N. H. Sabah,et al.  Cutaneous mechanoreceptors influencing impulse discharges in cerebellar cortex. I. In mossy fibers , 2004, Experimental Brain Research.

[42]  J. Bower,et al.  Congruence of spatial organization of tactile projections to granule cell and Purkinje cell layers of cerebellar hemispheres of the albino rat: vertical organization of cerebellar cortex. , 1983, Journal of neurophysiology.

[43]  R. Koeppe,et al.  Comparison of human cerebral activation pattern during cutaneous warmth, heat pain, and deep cold pain. , 1996, Journal of neurophysiology.

[44]  Kenneth O. Johnson,et al.  The roles and functions of cutaneous mechanoreceptors , 2001, Current Opinion in Neurobiology.

[45]  S. Francis,et al.  Mapping human somatosensory cortex in individual subjects with 7 T functional MRI 1 Running title : Mapping human somatosensory cortex , 2010 .

[46]  David D. Cox,et al.  Functional magnetic resonance imaging (fMRI) “brain reading”: detecting and classifying distributed patterns of fMRI activity in human visual cortex , 2003, NeuroImage.

[47]  Masao Ito Cerebellar learning in the vestibulo–ocular reflex , 1998, Trends in Cognitive Sciences.

[48]  J. Kaas,et al.  Multiple representations of the body within the primary somatosensory cortex of primates. , 1979, Science.

[49]  F. Tong,et al.  Decoding Seen and Attended Motion Directions from Activity in the Human Visual Cortex , 2006, Current Biology.

[50]  Jörn Diedrichsen,et al.  A spatially unbiased atlas template of the human cerebellum , 2006, NeuroImage.

[51]  R. Turner,et al.  Characterization and Correction of Interpolation Effects in the Realignment of fMRI Time Series , 2000, NeuroImage.

[52]  Guy Marchal,et al.  Automated multi-modality image registration based on information theory , 1995 .

[53]  J. Kaas,et al.  Variability in hand surface representations in areas 3b and 1 in adult owl and squirrel monkeys , 1987, The Journal of comparative neurology.

[54]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[55]  J. Kaas,et al.  Representations of the body surface in cortical areas 3b and 1 of squirrel monkeys: Comparisons with other primates , 1982, The Journal of comparative neurology.

[56]  Iole Indovina,et al.  On Somatotopic Representation Centers for Finger Movements in Human Primary Motor Cortex and Supplementary Motor Area , 2001, NeuroImage.

[57]  Karl J. Friston,et al.  Comparing the similarity and spatial structure of neural representations: A pattern-component model , 2011, NeuroImage.

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

[59]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[60]  T. Mima,et al.  Brain structures related to active and passive finger movements in man. , 1999, Brain : a journal of neurology.

[61]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[62]  E. S. Pearson Biometrika tables for statisticians , 1967 .

[63]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[64]  S. Kiebel,et al.  Multiple somatotopic representations in the human cerebellum. , 1999, Neuroreport.

[65]  Paul E. Downing,et al.  A comparison of volume-based and surface-based multi-voxel pattern analysis , 2011, NeuroImage.

[66]  G. Rees,et al.  Predicting the orientation of invisible stimuli from activity in human primary visual cortex , 2005, Nature Neuroscience.