Human Sensorimotor Cortex Represents Conflicting Visuomotor Mappings

Behavioral studies have shown that humans can adapt to conflicting sensorimotor mappings that cause interference after intensive training. While previous research works indicate the involvement of distinct brain regions for different types of motor learning (e.g., kinematics vs dynamics), the neural mechanisms underlying joint adaptation to conflicting mappings within the same type of perturbation (e.g., different angles of visuomotor rotation) remain unclear. To reveal the neural substrates that represent multiple sensorimotor mappings, we examined whether different mappings could be classified with multivoxel activity patterns of functional magnetic resonance imaging data. Participants simultaneously adapted to opposite rotational perturbations (+90° and − 90°) during visuomotor tracking. To dissociate differences in movement kinematics with rotation types, we used two distinct patterns of target motion and tested generalization of the classifier between different combinations of rotation and motion types. Results showed that the rotation types were classified significantly above chance using activities in the primary sensorimotor cortex and the supplementary motor area, despite no significant difference in averaged signal amplitudes within the region. In contrast, low-level sensorimotor components, including tracking error and movement speed, were best classified using activities of the early visual cortex. Our results reveal that the sensorimotor cortex represents different visuomotor mappings, which permits joint learning and switching between conflicting sensorimotor skills.

[1]  J. Krakauer,et al.  Differential cortical and subcortical activations in learning rotations and gains for reaching: a PET study. , 2004, Journal of neurophysiology.

[2]  E. Bizzi,et al.  Neuronal activity in the supplementary motor area of monkeys adapting to a new dynamic environment. , 2004, Journal of neurophysiology.

[3]  Jeremy Freeman,et al.  Orientation Decoding Depends on Maps, Not Columns , 2011, The Journal of Neuroscience.

[4]  J. Duncan,et al.  Top-Down Activation of Shape-Specific Population Codes in Visual Cortex during Mental Imagery , 2009, The Journal of Neuroscience.

[5]  P. Celnik,et al.  Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. , 2011, Cerebral cortex.

[6]  Hanna Damasio,et al.  Predicting visual stimuli on the basis of activity in auditory cortices , 2010, Nature Neuroscience.

[7]  Toshio Inui,et al.  Neural representation of observed actions in the parietal and premotor cortex , 2011, NeuroImage.

[8]  R. Miall,et al.  Digital Object Identifier (DOI) 10.1007/s002219900286 RESEARCH ARTICLE , 2022 .

[9]  Alfonso Caramazza,et al.  Tuning Curves for Movement Direction in the Human Visuomotor System , 2010, The Journal of Neuroscience.

[10]  Fraser W. Smith,et al.  Decoding Effector-Dependent and Effector-Independent Movement Intentions from Human Parieto-Frontal Brain Activity , 2011, The Journal of Neuroscience.

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

[12]  Christian Keysers,et al.  Testing Simulation Theory with Cross-Modal Multivariate Classification of fMRI Data , 2008, PloS one.

[13]  John W. Krakauer,et al.  Independent learning of internal models for kinematic and dynamic control of reaching , 1999, Nature Neuroscience.

[14]  R B Welch,et al.  Multiple concurrent visual-motor mappings: implications for models of adaptation. , 1994, Journal of experimental psychology. Human perception and performance.

[15]  R. Miall,et al.  Task-dependent changes in visual feedback control: a frequency analysis of human manual tracking. , 1996, Journal of motor behavior.

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

[17]  H. Kennedy,et al.  Two Cortical Systems for Reaching in Central and Peripheral Vision , 2005, Neuron.

[18]  Takeo Watanabe,et al.  Perceptual learning incepted by decoded fMRI neurofeedback without stimulus presentation , 2012 .

[19]  Toshio Inui,et al.  Reference Frame of Human Medial Intraparietal Cortex in Visually Guided Movements , 2012, Journal of Cognitive Neuroscience.

[20]  D Timmann,et al.  Adaptation to visuomotor rotation and force field perturbation is correlated to different brain areas in patients with cerebellar degeneration. , 2009, Journal of neurophysiology.

[21]  N. Schweighofer,et al.  Dual Adaptation Supports a Parallel Architecture of Motor Memory , 2009, The Journal of Neuroscience.

[22]  E. Vaadia,et al.  Preparatory activity in motor cortex reflects learning of local visuomotor skills , 2003, Nature Neuroscience.

[23]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[24]  B. T. Thomas Yeo,et al.  Integration of sensory and motor representations of single fingers in the human cerebellum , 2011 .

[25]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[26]  J. Krakauer,et al.  Are We Ready for a Natural History of Motor Learning? , 2011, Neuron.

[27]  Patrik Vuilleumier,et al.  Felt and Seen Pain Evoke the Same Local Patterns of Cortical Activity in Insular and Cingulate Cortex , 2011, The Journal of Neuroscience.

[28]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.

[29]  Zoubin Ghahramani,et al.  Modular decomposition in visuomotor learning , 1997, Nature.

[30]  M. Kawato,et al.  Acquisition and contextual switching of multiple internal models for different viscous force fields , 2003, Neuroscience Research.

[31]  Bogdan Draganski,et al.  Neuroplasticity: Changes in grey matter induced by training , 2004, Nature.

[32]  S. Scott The role of primary motor cortex in goal-directed movements: insights from neurophysiological studies on non-human primates , 2003, Current Opinion in Neurobiology.

[33]  M. Kawato,et al.  Modular organization of internal models of tools in the human cerebellum , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[35]  Hagai Bergman,et al.  Emerging Patterns of Neuronal Responses in Supplementary and Primary Motor Areas during Sensorimotor Adaptation , 2005, The Journal of Neuroscience.

[36]  Gereon R. Fink,et al.  Human medial intraparietal cortex subserves visuomotor coordinate transformation , 2004, NeuroImage.

[37]  Daniel A. Braun,et al.  Motor Task Variation Induces Structural Learning , 2009, Current Biology.

[38]  Alison J. Wiggett,et al.  Surface-Based Information Mapping Reveals Crossmodal Vision–Action Representations in Human Parietal and Occipitotemporal Cortex , 2010, Journal of neurophysiology.

[39]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

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

[41]  Nicolas Schweighofer,et al.  Performance-Based Adaptive Schedules Enhance Motor Learning , 2008, Journal of motor behavior.

[42]  Reza Shadmehr,et al.  Impairment of Retention But Not Acquisition of a Visuomotor Skill Through Time-Dependent Disruption of Primary Motor Cortex , 2007, The Journal of Neuroscience.

[43]  M. Kawato,et al.  Behavioral/systems/cognitive Functional Magnetic Resonance Imaging Examination of Two Modular Architectures for Switching Multiple Internal Models , 2022 .

[44]  M. Kawato,et al.  Random presentation enables subjects to adapt to two opposing forces on the hand , 2004, Nature Neuroscience.

[45]  Valeria Della-Maggiore,et al.  One Week of Motor Adaptation Induces Structural Changes in Primary Motor Cortex That Predict Long-Term Memory One Year Later , 2011, The Journal of Neuroscience.

[46]  Otmar Bock,et al.  An fMRI study of brain activation in a visual adaptation task: activation limited to sensory guidance , 2008, Experimental Brain Research.

[47]  V. Michel,et al.  Recruitment of an Area Involved in Eye Movements During Mental Arithmetic , 2009, Science.

[48]  E. Vaadia,et al.  Single Neurons in M1 and Premotor Cortex Directly Reflect Behavioral Interference , 2012, PloS one.

[49]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[50]  Justin L. Gardner,et al.  Executed and Observed Movements Have Different Distributed Representations in Human aIPS , 2008, The Journal of Neuroscience.

[51]  Ian S Howard,et al.  Composition and Decomposition in Bimanual Dynamic Learning , 2008, The Journal of Neuroscience.

[52]  D M Wolpert,et al.  Multiple paired forward and inverse models for motor control , 1998, Neural Networks.

[53]  Justin L. Gardner,et al.  Is cortical vasculature functionally organized? , 2010, NeuroImage.

[54]  Ravi S. Menon,et al.  Learning-related fMRI activation associated with a rotational visuo-motor transformation. , 2005, Brain research. Cognitive brain research.

[55]  Paul Sacco,et al.  Modulation of internal model formation during force field‐induced motor learning by anodal transcranial direct current stimulation of primary motor cortex , 2009, The Journal of physiology.

[56]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[57]  Hiroshi Imamizu,et al.  Human cerebellar activity reflecting an acquired internal model of a new tool , 2000, Nature.

[58]  S. Wise,et al.  Changes in motor cortical activity during visuomotor adaptation , 1998, Experimental Brain Research.

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

[60]  J Randall Flanagan,et al.  Visuomotor rotations of varying size and direction compete for a single internal model in motor working memory. , 2002, Journal of experimental psychology. Human perception and performance.

[61]  Ehud Zohary,et al.  Functional Organization of Human Motor Cortex: Directional Selectivity for Movement , 2010, The Journal of Neuroscience.

[62]  D C Noll,et al.  Neuroanatomical correlates of motor acquisition and motor transfer. , 2008, Journal of neurophysiology.

[63]  Soyoung Q. Park,et al.  Decoding the Formation of Reward Predictions across Learning , 2011, The Journal of Neuroscience.

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

[65]  M. Kawato,et al.  Explicit contextual information selectively contributes to predictive switching of internal models , 2007, Experimental Brain Research.

[66]  Andreas Bartels,et al.  fMRI and its interpretations: an illustration on directional selectivity in area V5/MT , 2008, Trends in Neurosciences.

[67]  S. Kinomura,et al.  A PET Study of Visuomotor Learning under Optical Rotation , 2000, NeuroImage.

[68]  Denis Schluppeck,et al.  Contribution of large scale biases in decoding of direction-of-motion from high-resolution fMRI data in human early visual cortex , 2012, NeuroImage.

[69]  Jörn Diedrichsen,et al.  Two Distinct Ipsilateral Cortical Representations for Individuated Finger Movements , 2012, Cerebral cortex.

[70]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[71]  Eilon Vaadia,et al.  Specificity of sensorimotor learning and the neural code: Neuronal representations in the primary motor cortex , 2004, Journal of Physiology-Paris.

[72]  John W Krakauer,et al.  Adaptation to visuomotor rotation through interaction between posterior parietal and motor cortical areas. , 2009, Journal of neurophysiology.

[73]  M. Kawato,et al.  Reorganization of Brain Activity for Multiple Internal Models After Short But Intensive Training , 2007, Cortex.

[74]  Stephen H Scott,et al.  Limited transfer of learning between unimanual and bimanual skills within the same limb , 2006, Nature Neuroscience.

[75]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[76]  Kenneth F. Valyear,et al.  Decoding Action Intentions from Preparatory Brain Activity in Human Parieto-Frontal Networks , 2011, The Journal of Neuroscience.

[77]  Ehud Zohary,et al.  The Representation of Visual and Motor Aspects of Reaching Movements in the Human Motor Cortex , 2011, The Journal of Neuroscience.