Intracortical Microstimulation Maps of Motor, Somatosensory, and Posterior Parietal Cortex in Tree Shrews (Tupaia belangeri) Reveal Complex Movement Representations

Abstract Long‐train intracortical microstimulation (LT‐ICMS) is a popular method for studying the organization of motor and posterior parietal cortex (PPC) in mammals. In primates, LT‐ICMS evokes both multijoint and multiple‐body‐part movements in primary motor, premotor, and PPC. In rodents, LT‐ICMS evokes complex movements of a single limb in motor cortex. Unfortunately, very little is known about motor/PPC organization in other mammals. Tree shrews are closely related to both primates and rodents and could provide insights into the evolution of complex movement domains in primates. The present study investigated the extent of cortex in which movements could be evoked with ICMS and the characteristics of movements elicited using both short train (ST) and LT‐ICMS in tree shrews. We demonstrate that LT‐ICMS and ST‐ICMS maps are similar, with the movements elicited with ST‐ICMS being truncated versions of those elicited with LT‐ICMS. In addition, LT‐ICMS‐evoked complex movements within motor cortex similar to those in rodents. More complex movements involving multiple body parts such as the hand and mouth were also elicited in motor cortex and PPC, as in primates. Our results suggest that complex movement networks present in PPC and motor cortex were present in mammals prior to the emergence of primates.

[1]  J. Buettner‐Janusch The Antecedents of Man , 1963, The Yale Journal of Biology and Medicine.

[2]  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.

[3]  Paul D Cheney,et al.  Effective intracortical microstimulation parameters applied to primary motor cortex for evoking forelimb movements to stable spatial end points. , 2013, Journal of neurophysiology.

[4]  Andrew R. Brown,et al.  Motor Cortex Is Functionally Organized as a Set of Spatially Distinct Representations for Complex Movements , 2014, The Journal of Neuroscience.

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

[6]  Simon A. Overduin,et al.  Microstimulation Activates a Handful of Muscle Synergies , 2012, Neuron.

[7]  Y. Gioanni,et al.  A reappraisal of rat motor cortex organization by intracortical microstimulation , 1985, Brain Research.

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

[9]  K. Zilles,et al.  Functional neuroanatomy of the primate isocortical motor system , 2000, Anatomy and Embryology.

[10]  E. Neafsey,et al.  A second forelimb motor area exists in rat frontal cortex , 1982, Brain Research.

[11]  Tirin Moore,et al.  Complex movements evoked by microstimulation of the ventral intraparietal area , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  C. Campbell,et al.  The Origin of the Corticospinal Tract of the Tree Shrew (Tupaia glis) with Observations on Its Brain Stem and Spinal Terminations , 1969 .

[13]  D. N. Lenkov,et al.  Functional mapping of the motor cortex of the white mouse by a microstimulation method , 2006, Neuroscience and Behavioral Physiology.

[14]  Jon H Kaas,et al.  Architectonic Subdivisions of Neocortex in the Tree Shrew (Tupaia belangeri) , 2009, Anatomical record.

[15]  Timothy H. Murphy,et al.  Distinct Cortical Circuit Mechanisms for Complex Forelimb Movement and Motor Map Topography , 2012, Neuron.

[16]  J. Kaas,et al.  Architectionis, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys , 1993, The Journal of comparative neurology.

[17]  Iwona Stepniewska,et al.  Thalamocortical connections of functional zones in posterior parietal cortex and frontal cortex motor regions in New World monkeys. , 2010, Cerebral cortex.

[18]  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.

[19]  Iwona Stepniewska,et al.  Optical imaging in galagos reveals parietal–frontal circuits underlying motor behavior , 2011, Proceedings of the National Academy of Sciences.

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

[21]  G. Rizzolatti,et al.  The fronto-parietal cortex of the prosimian Galago: Patterns of cytochrome oxidase activity and motor maps , 1994, Behavioural Brain Research.

[22]  D. Ferrier Experiments on the brain of monkeys.—No. I , 1875, Proceedings of the Royal Society of London.

[23]  Dylan F. Cooke,et al.  The Cortical Control of Movement Revisited , 2002, Neuron.

[24]  M. Desmurget,et al.  Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus , 2014, Proceedings of the National Academy of Sciences.

[25]  D. Boyer,et al.  Intrinsic hand proportions of euarchontans and other mammals: implications for the locomotor behavior of plesiadapiforms. , 2008, Journal of human evolution.

[26]  H. Sakata,et al.  Functional Organization of a Cortical Efferent System Examined with Focal Depth Stimulation in Cats , 1967 .

[27]  H C Kwan,et al.  Spatial organization of precentral cortex in awake primates. II. Motor outputs. , 1978, Journal of neurophysiology.

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

[29]  Iwona Stepniewska,et al.  Cortical connections of functional zones in posterior parietal cortex and frontal cortex motor regions in new world monkeys. , 2011, Cerebral cortex.

[30]  E. J. Sargis The grasping behaviour, locomotion and substrate use of the tree shrews Tupaia minor and T. tana (Mammalia, Scandentia) , 2001 .

[31]  R. Hira,et al.  Distinct Functional Modules for Discrete and Rhythmic Forelimb Movements in the Mouse Motor Cortex , 2015, The Journal of Neuroscience.

[32]  R. Nudo,et al.  Descending pathways to the spinal cord, III: Sites of origin of the corticospinal tract , 1990, The Journal of comparative neurology.

[33]  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.

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

[35]  R P Lesser,et al.  Localization of sensorimotor cortex: the influence of Sherrington and Cushing on the modern concept. , 1992, Neurosurgery.

[36]  Iwona Stepniewska,et al.  Organization of the posterior parietal cortex in galagos: II. Ipsilateral cortical connections of physiologically identified zones within anterior sensorimotor region , 2009, The Journal of comparative neurology.

[37]  J. Kaas,et al.  Subdivisions of the visual system labeled with the Cat-301 antibody in tree shrews , 1994, Visual Neuroscience.

[38]  J. Kaas,et al.  Microstimulation and architectonics of frontoparietal cortex in common marmosets (Callithrix jacchus) , 2008, The Journal of comparative neurology.

[39]  J. G. D. D. Barenne CENTRAL LEVELS OF SENSORY INTEGRATION , 1935 .

[40]  Jamie L. Reed,et al.  Organization of frontoparietal cortex in the tree shrew (Tupaia belangeri). I. Architecture, microelectrode maps, and corticospinal connections , 2006, The Journal of comparative neurology.

[41]  J. Donoghue,et al.  Organization of the forelimb area in squirrel monkey motor cortex: representation of digit, wrist, and elbow muscles , 2004, Experimental Brain Research.

[42]  C. Woolsey,et al.  Sensory and motor localization in cerebral cortex of porcupine (Erethizon dorsatum). , 1956, Journal of neurophysiology.

[43]  W. D. Thompson,et al.  Excitation of pyramidal tract cells by intracortical microstimulation: effective extent of stimulating current. , 1968, Journal of neurophysiology.

[44]  I. H. Coriat,et al.  Histological Studies on the Localization of Cerebral Function , 1906 .

[45]  Dylan F. Cooke,et al.  Arm movements evoked by electrical stimulation in the motor cortex of monkeys. , 2005, Journal of neurophysiology.

[46]  M. Wiesendanger,et al.  Structural and functional definition of the motor cortex in the monkey (Macaca fascicularis) , 1982, The Journal of physiology.

[47]  N. P. Bichot,et al.  Converging evidence from microstimulation, architecture, and connections for multiple motor areas in the frontal and cingulate cortex of prosimian primates , 2000, The Journal of comparative neurology.

[48]  Peter L. Strick,et al.  Stimulating research on motor cortex , 2002, Nature Neuroscience.

[49]  R. Lende,et al.  Cortical localization in the tree shrew (Tupaia). , 1970, Brain research.

[50]  Iwona Stepniewska,et al.  Cortical Networks for Ethologically Relevant Behaviors in Primates , 2013, American journal of primatology.

[51]  Dylan F. Cooke,et al.  The functional organization and cortical connections of motor cortex in squirrels. , 2012, Cerebral cortex.

[52]  R. S. Waters,et al.  Organization of the Mouse Motor Cortex Studied by Retrograde Tracing and Intracortical Microstimulation (ICMS) Mapping , 1991, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[53]  Cizhong Jiang,et al.  Phylogenetic affinity of tree shrews to Glires is attributed to fast evolution rate. , 2014, Molecular phylogenetics and evolution.

[54]  L. Bonazzi,et al.  Complex Movement Topography and Extrinsic Space Representation in the Rat Forelimb Motor Cortex as Defined by Long-Duration Intracortical Microstimulation , 2013, The Journal of Neuroscience.

[55]  J. Kaas,et al.  The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and the frontal eye fields in owl monkeys , 1986, The Journal of comparative neurology.

[56]  M. Tuszynski,et al.  A form of motor cortical plasticity that correlates with recovery of function after brain injury. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Paul D Cheney,et al.  EMG Activation Patterns Associated with High Frequency, Long-Duration Intracortical Microstimulation of Primary Motor Cortex , 2014, The Journal of Neuroscience.

[58]  Iwona Stepniewska,et al.  Effects of muscimol inactivations of functional domains in motor, premotor, and posterior parietal cortex on complex movements evoked by electrical stimulation. , 2014, Journal of neurophysiology.

[59]  B. Kolb,et al.  Functional Organization of Rat and Mouse Motor Cortex , 2011 .

[60]  Iwona Stepniewska,et al.  Organization of the posterior parietal cortex in galagos: I. Functional zones identified by microstimulation , 2009, The Journal of comparative neurology.

[61]  J. B. Preston,et al.  Two representations of the hand in area 4 of a primate. I. Motor output organization. , 1982, Journal of neurophysiology.

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

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

[64]  C. S. Sherrington,et al.  An ADDRESS on LOCALISATION in the “MOTOR” CEREBRAL CORTEX , 1901, British medical journal.

[65]  F. Jenkins 3 – Tree Shrew Locomotion and the Origins of Primate Arborealism* , 1974 .

[66]  J. Kaas,et al.  Cortical connections of striate and extrastriate visual areas in tree shrews , 1998, The Journal of comparative neurology.

[67]  W. L. Clark The antecedents of man , 1959 .

[68]  J. Kaas,et al.  Cortical networks subserving upper limb movements in primates. , 2012, European journal of physical and rehabilitation medicine.

[69]  Celine Mateo,et al.  Motor Control by Sensory Cortex , 2010, Science.

[70]  M. Graziano The Intelligent Movement Machine: An Ethological Perspective on the Primate Motor System , 2008 .

[71]  E. Rouiller,et al.  Comparison of the connectional properties of the two forelimb areas of the rat sensorimotor cortex: support for the presence of a premotor or supplementary motor cortical area. , 1993, Somatosensory & motor research.

[72]  Iwona Stepniewska,et al.  Multiple Parietal–Frontal Pathways Mediate Grasping in Macaque Monkeys , 2011, The Journal of Neuroscience.

[73]  C. Sherrington,et al.  OBSERVATIONS ON THE EXCITABLE CORTEX OF THE CHIMPANZEE, ORANG‐UTAN, AND GORILLA , 1917 .

[74]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[75]  Iwona Stepniewska,et al.  Microstimulation reveals specialized subregions for different complex movements in posterior parietal cortex of prosimian galagos. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[76]  David C Lyon,et al.  The organization of frontoparietal cortex in the tree shrew (Tupaia belangeri): II. Connectional evidence for a frontal‐posterior parietal network , 2007, The Journal of comparative neurology.

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

[78]  P. Cheney,et al.  Equilibrium-Based Movement Endpoints Elicited from Primary Motor Cortex Using Repetitive Microstimulation , 2014, The Journal of Neuroscience.

[79]  Iwona Stepniewska,et al.  Evolution of posterior parietal cortex and parietal‐frontal networks for specific actions in primates , 2016, The Journal of comparative neurology.

[80]  T. Yin,et al.  Visual response properties of neurons in the middle and lateral suprasylvian cortices of the behaving cat , 2005, Experimental Brain Research.

[81]  R P Lesser,et al.  Does the central sulcus divide motor and sensory functions , 1996, Neurology.