The Neural Representation of Kinematics and Dynamics in Multiple Brain Regions: The Use of Force Field Reaching Paradigms in the Primate and Rat

In this chapter I will review the past and present motor control literature with an emphasis on reaching movements. Debate still rages as to what movement related variables are controlled by the neural motor control system especially concerning dynamic vs. kinematic variables. There is a rich history in the motor control literature that has employed monkeys of several species making reaching movements while holding loaded or robotic manipulandum. However, to date very little work has been conducted using the rat reaching paradigm to investigate the control of dynamics vs. kinematics. I will review a very simple rat robotic manipulandum paradigm and initial results from it. This paradigm is presently being expanded from a 1 degree of freedom system similar to those used in early primate research to a 2 and even 3 degree of freedom version, such as those used with primates and humans today.

[1]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. III. Positional gradients and population coding of movement direction from various movement origins , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  R. Nelson.  The Somatosensory System , 2001 .

[3]  R. Sacco,et al.  Selective proprioceptive loss from a thalamic lacunar stroke. , 1987, Stroke.

[4]  F. J. Clark,et al.  Slowly adapting receptors in cat knee joint: can they signal joint angle? , 1975, Journal of neurophysiology.

[5]  F. Vidal,et al.  Programming response duration in a precueing reaction time paradigm. , 1991, Journal of motor behavior.

[6]  C. Fromm,et al.  Static firing rates of premotor and primary motor cortical neurons associated with torque and joint position , 2004, Experimental Brain Research.

[7]  J. Chapin,et al.  Proprioceptive and cutaneous representations in the rat ventral posterolateral thalamus. , 2008, Journal of neurophysiology.

[8]  Joseph T. Francis,et al.  Force field apparatus for investigating movement control in small animals , 2004, IEEE Transactions on Biomedical Engineering.

[9]  Dawn M. Taylor,et al.  Direct Cortical Control of 3D Neuroprosthetic Devices , 2002, Science.

[10]  A. Schwartz.  Motor cortical activity during drawing movements: single-unit activity during sinusoid tracing. , 1992, Journal of neurophysiology.

[11]  W A MacKay,et al.  CNV, stretch reflex and reaction time correlates of preparation for movement direction and force. , 1990, Electroencephalography and clinical neurophysiology.

[12]  J. Kaas,et al.  Ablations of areas 3b (SI proper) and 3a of somatosensory cortex in marmosets deactivate the second and parietal ventral somatosensory areas. , 1990, Somatosensory & motor research.

[13]  John Nolte,et al.  The Human Brain An Introduction to Its Functional Anatomy , 2013 .

[14]  Philip N. Sabes,et al.  Multisensory Integration during Motor Planning , 2003, The Journal of Neuroscience.

[15]  Alexa Riehle,et al.  Neuronal correlates of the specification of movement direction and force in four cortical areas of the monkey , 1995, Behavioural Brain Research.

[16]  E. Fetz,et al.  Operant Conditioning of Specific Patterns of Neural and Muscular Activity , 1971, Science.

[17]  E. Bizzi,et al.  Neuronal Correlates of Motor Performance and Motor Learning in the Primary Motor Cortex of Monkeys Adapting to an External Force Field , 2001, Neuron.

[18]  Andrew B. Schwartz,et al.  Brain-Controlled Interfaces: Movement Restoration with Neural Prosthetics , 2006, Neuron.

[19]  S. Scott,et al.  Changes in motor cortex activity during reaching movements with similar hand paths but different arm postures. , 1995, Journal of neurophysiology.

[20]  J. Kalaska,et al.  Motor cortex neural correlates of output kinematics and kinetics during isometric-force and arm-reaching tasks. , 2005, Journal of neurophysiology.

[21]  A B Schwartz,et al.  Motor cortical representation of speed and direction during reaching. , 1999, Journal of neurophysiology.

[22]  William J Kargo,et al.  Improvements in the Signal-to-Noise Ratio of Motor Cortex Cells Distinguish Early versus Late Phases of Motor Skill Learning , 2004, The Journal of Neuroscience.

[23]  J. Gordon,et al.  Impairments of reaching movements in patients without proprioception. I. Spatial errors. , 1995, Journal of neurophysiology.

[24]  J. Eian,et al.  Kinematic and non-kinematic signals transmitted to the cat cerebellum during passive treadmill stepping , 2005, Experimental Brain Research.

[25]  G. Grant.  Projection of the external cuneate nucleus onto the cerebellum in the cat: an experimental study using silver methods. , 1962, Experimental neurology.

[26]  R. Lemon,et al.  Contribution of the monkey corticomotoneuronal system to the control of force in precision grip. , 1993, Journal of neurophysiology.

[27]  I. Whishaw.  An endpoint, descriptive, and kinematic comparison of skilled reaching in mice (Mus musculus) with rats (Rattus norvegicus) , 1996, Behavioural Brain Research.

[28]  J. Kaas,et al.  Regional segregation of neurons responding to quickly adapting, slowly adapting, deep and pacinian receptors within thalamic ventroposterior lateral and ventroposterior inferior nuclei in the squirrel monkey (Saimiri sciureus) , 1981, Neuroscience.

[29]  M S Graziano,et al.  Coding the location of the arm by sight. , 2000, Science.

[30]  J. Gordon,et al.  Impairments of reaching movements in patients without proprioception. II. Effects of visual information on accuracy. , 1995, Journal of neurophysiology.

[31]  S Grossberg,et al.  A model of movement coordinates in the motor cortex: posture-dependent changes in the gain and direction of single cell tuning curves. , 2001, Cerebral cortex.

[32]  J. T. Massey,et al.  Interruption of motor cortical discharge subserving aimed arm movements , 1983, Experimental Brain Research.

[33]  Philip N. Sabes,et al.  Flexible strategies for sensory integration during motor planning , 2005, Nature Neuroscience.

[34]  J. Kalaska,et al.  Systematic changes in motor cortex cell activity with arm posture during directional isometric force generation. , 2003, Journal of neurophysiology.

[35]  E. Moberg.  The role of cutaneous afferents in position sense, kinaesthesia, and motor function of the hand. , 1983, Brain : a journal of neurology.

[36]  F. J. Clark,et al.  Characteristics of knee joint receptors in the cat , 1969, The Journal of physiology.

[37]  S. Scott,et al.  Reaching movements with similar hand paths but different arm orientations. I. Activity of individual cells in motor cortex. , 1997, Journal of neurophysiology.

[38]  Joseph T. Francis.  Error generalization as a function of velocity and duration: human reaching movements , 2007, Experimental Brain Research.

[39]  O. I. Fukson,et al.  Origin of modulation in neurones of the ventral spinocerebellar tract during locomotion. , 1972, Brain research.

[40]  Jerald D. Kralik,et al.  Real-time prediction of hand trajectory by ensembles of cortical neurons in primates , 2000, Nature.

[41]  Reza Shadmehr,et al.  Learning of action through adaptive combination of motor primitives , 2000, Nature.

[42]  E. Bizzi,et al.  Neuronal correlates of movement dynamics in the dorsal and ventral premotor area in the monkey , 2005, Experimental Brain Research.

[43]  David M. Santucci,et al.  Learning to Control a Brain–Machine Interface for Reaching and Grasping by Primates , 2003, PLoS biology.

[45]  J. Wann,et al.  Does limb proprioception drift? , 2004, Experimental Brain Research.

[46]  C. Gauriau,et al.  A comparative reappraisal of projections from the superficial laminae of the dorsal horn in the rat: The forebrain , 2004, The Journal of comparative neurology.

[47]  E. Evarts.  Activity of pyramidal tract neurons during postural fixation. , 1969, Journal of neurophysiology.

[48]  A. Georgopoulos,et al.  On the relations between single cell activity in the motor cortex and the direction and magnitude of three-dimensional static isometric force , 2004, Experimental Brain Research.

[49]  J. Kaas,et al.  What, if anything, is SI? Organization of first somatosensory area of cortex. , 1983, Physiological reviews.

[50]  J. Lackner,et al.  Rapid adaptation to Coriolis force perturbations of arm trajectory. , 1994, Journal of neurophysiology.

[51]  L A Krubitzer,et al.  The somatosensory thalamus of monkeys: Cortical connections and a redefinition of nuclei in marmosets , 1992, The Journal of comparative neurology.

[52]  Nicholas G. Hatsopoulos,et al.  Brain-machine interface: Instant neural control of a movement signal , 2002, Nature.

[53]  Ian Q. Whishaw,et al.  The impairments in reaching and the movements of compensation in rats with motor cortex lesions: an endpoint, videorecording, and movement notation analysis , 1991, Behavioural Brain Research.

[54]  K W Horch,et al.  A chronic intracortical electrode array: preliminary results. , 1989, Journal of biomedical materials research.

[55]  W. Kargo,et al.  Early Skill Learning Is Expressed through Selection and Tuning of Cortically Represented Muscle Synergies , 2003, The Journal of Neuroscience.

[56]  R. Poppele,et al.  Reference frames for spinal proprioception: kinematics based or kinetics based? , 2000, Journal of neurophysiology.

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

[58]  R. M. Siegel,et al.  Encoding of spatial location by posterior parietal neurons. , 1985, Science.

[59]  E. Fetz,et al.  Functional classes of primate corticomotoneuronal cells and their relation to active force. , 1980, Journal of neurophysiology.

[60]  D. Weber,et al.  Coding of position by simultaneously recorded sensory neurones in the cat dorsal root ganglion , 2004, The Journal of physiology.

[61]  J. Kalaska,et al.  A comparison of movement direction-related versus load direction- related activity in primate motor cortex, using a two-dimensional reaching task , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  V. Perciavalle,et al.  Anisotropic representation of forelimb position in the cerebellar cortex and nucleus interpositus of the rat , 2003, Brain Research.

[63]  E. Todorov.  Direct cortical control of muscle activation in voluntary arm movements: a model , 2000, Nature Neuroscience.

[64]  S. Scott,et al.  Random change in cortical load representation suggests distinct control of posture and movement , 2005, Nature Neuroscience.

[65]  J.T. Francis,et al.  Neural ensemble activity from multiple brain regions predicts kinematic and dynamic variables in a multiple force field reaching task , 2006, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[66]  R. Poppele,et al.  Proprioception from a spinocerebellar perspective. , 2001, Physiological reviews.

[67]  J. Soechting,et al.  Somatosensory cortical activity in relation to arm posture: nonuniform spatial tuning. , 1996, Journal of neurophysiology.

[68]  Ferdinando A Mussa-Ivaldi,et al.  Interaction of visual and proprioceptive feedback during adaptation of human reaching movements. , 2005, Journal of neurophysiology.

[69]  R. Poppele,et al.  Phase-specific sensory representations in spinocerebellar activity during stepping: evidence for a hybrid kinematic/kinetic framework , 2006, Experimental Brain Research.

[70]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during lemniscate tracing. , 1999 .

[71]  J. Kalaska,et al.  Proprioceptive activity in primate primary somatosensory cortex during active arm reaching movements. , 1994, Journal of neurophysiology.

[72]  A. Schwartz,et al.  On the relationship between joint angular velocity and motor cortical discharge during reaching. , 2001, Journal of neurophysiology.

[73]  O. Oscarsson,et al.  IDENTIFICATION OF A SPINOCEREBELLAR TRACT ACTIVATED FROM FORELIMB AFFERENTS IN THE CAT. , 1964, Acta physiologica Scandinavica.

[74]  F. A. Mussa-lvaldi,et al.  Convergent force fields organized in the frog's spinal cord , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[75]  R A Normann,et al.  A 100 electrode intracortical array: structural variability. , 1990, Biomedical sciences instrumentation.

[76]  J. Kaas,et al.  The Organization of the Somatosensory System in Primates , 2001 .

[77]  K. A. Clarke,et al.  An analysis of the representation of the forelimb in the ventrobasal thalamic complex of the albino rat. , 1975, The Journal of physiology.

[78]  E. Bizzi,et al.  Characteristics of motor programs underlying arm movements in monkeys. , 1979, Journal of neurophysiology.

[79]  A. Lundberg.  Function of the ventral spinocerebellar tract a new hypothesis , 2004, Experimental Brain Research.

[80]  S. Meagher.  Instant neural control of a movement signal , 2002 .

[81]  J. Ashe.  Erratum to “Force and the motor cortex” [Behavioural Brain Research 86 (1997) 1–15] 1 PII of original article: S0166-4328(96)00145-3 1 , 1997, Behavioural Brain Research.

[82]  O. I. Fukson,et al.  Recordings of neurones of the dorsal spinocerebellar tract during evoked locomotion. , 1972, Brain research.

[83]  P R Kennedy,et al.  Direct control of a computer from the human central nervous system. , 2000, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[84]  D. Rosenbaum.  Human movement initiation: specification of arm, direction, and extent. , 1980, Journal of experimental psychology. General.

[85]  A. P. Georgopoulos,et al.  Cortical mechanisms related to the direction of two-dimensional arm movements: relations in parietal area 5 and comparison with motor cortex , 1983, Experimental Brain Research.

[86]  J. Vercher,et al.  Target and hand position information in the online control of goal-directed arm movements , 2003, Experimental Brain Research.

[87]  J. H. Kaas,et al.  Ablations of areas 3a and 3b of monkey somatosensory cortex abolish cutaneous responsivity in area 1 , 1990, Brain Research.

[88]  D. McCloskey,et al.  The role of joint receptors in human kinaesthesia when intramuscular receptors cannot contribute. , 1987, The Journal of physiology.

[89]  A. Craig,et al.  Retrograde analyses of spinothalamic projections in the macaque monkey: Input to posterolateral thalamus , 2006, The Journal of comparative neurology.

[90]  E. Evarts.  Pyramidal tract activity associated with a conditioned hand movement in the monkey. , 1966, Journal of neurophysiology.

[91]  J. Kalaska,et al.  Differential relation of discharge in primary motor cortex and premotor cortex to movements versus actively maintained postures during a reaching task , 1996, Experimental Brain Research.

[92]  G E Alexander,et al.  Movement-related neuronal activity selectively coding either direction or muscle pattern in three motor areas of the monkey. , 1990, Journal of neurophysiology.

[93]  J F Kalaska,et al.  Systematic changes in directional tuning of motor cortex cell activity with hand location in the workspace during generation of static isometric forces in constant spatial directions. , 1997, Journal of neurophysiology.

[94]  Separate representations of static and dynamic touch in human somatosensory thalamus , 2000, Neurology.

[95]  F A Mussa-Ivaldi,et al.  Adaptive representation of dynamics during learning of a motor task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[96]  J. Ashe.  Force and the motor cortex , 1997, Behavioural Brain Research.

[97]  W I Welker,et al.  Principles of organization of the ventrobasal complex in mammals. , 1973, Brain, behavior and evolution.

[98]  D. Hoffman,et al.  Muscle and movement representations in the primary motor cortex. , 1999, Science.

[99]  Reza Shadmehr,et al.  Quantifying Generalization from Trial-by-Trial Behavior of Adaptive Systems that Learn with Basis Functions: Theory and Experiments in Human Motor Control , 2003, The Journal of Neuroscience.

[100]  Ian Q. Whishaw,et al.  Olfaction directs skilled forelimb reaching in the rat , 1989, Behavioural Brain Research.

[101]  Vincenzo Perciavalle,et al.  Cerebellar encoding of limb position , 2008, The Cerebellum.

[102]  Ian Q. Whishaw,et al.  The structure of skilled forelimb reaching in the rat: A proximally driven movement with a single distal rotatory component , 1990, Behavioural Brain Research.

[103]  Kofman Eb,et al.  Interaction and joint precipitation of meromyosins with actin , 1966 .

[104]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[105]  Ian Q Whishaw,et al.  Skilled forelimb reaching for pasta guided by tactile input in the rat as measured by accuracy, spatial adjustments, and force , 2000, Behavioural Brain Research.

[106]  S. Scott,et al.  Neural activity in primary motor cortex related to mechanical loads applied to the shoulder and elbow during a postural task. , 2001, Journal of neurophysiology.

[107]  J. Yokota,et al.  Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey , 1981, Neuroscience Letters.

[108]  Timothy J. Ebner,et al.  Task dependence of primate arm postures , 1995, Experimental Brain Research.

[109]  Y. Amit,et al.  Encoding of Movement Fragments in the Motor Cortex , 2007, The Journal of Neuroscience.

[110]  G E Alexander,et al.  Neural representations of the target (goal) of visually guided arm movements in three motor areas of the monkey. , 1990, Journal of neurophysiology.

[111]  J. Vercher,et al.  Online control of the direction of rapid reaching movements , 2004, Experimental Brain Research.

[112]  F. Lacquaniti,et al.  Early coding of reaching in the parietooccipital cortex. , 2000, Journal of neurophysiology.

[113]  W. Welker.  Principles of Organization of the Ventrobasal Complex in Mammals; pp. 253–269 , 1973 .

[114]  G. E. Alexander,et al.  Preparation for movement: neural representations of intended direction in three motor areas of the monkey. , 1990, Journal of neurophysiology.

[115]  R E Poppele,et al.  Modulation of dorsal spinocerebellar responses to limb movement. I. Effect of serotonin. , 2003, Journal of neurophysiology.

[116]  A. Georgopoulos,et al.  Static spatial effects in motor cortex and area 5: Quantitative relations in a two-dimensional space , 1984, Experimental Brain Research.

[117]  A. Lundberg,et al.  Functional organization of connexions to the ventral spinocerebellar tract , 2004, Experimental Brain Research.

[118]  Yuval Yanai,et al.  Coordinate Transformation is First Completed Downstream of Primary Motor Cortex , 2008, The Journal of Neuroscience.

[119]  M. Graziano.  Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[120]  M. Pshirkov,et al.  Weak microlensing effect and stability of pulsar time scale , 2006, astro-ph/0610681.

[121]  Fel'dman Ag.  On the functional tuning of the nervous system in movement control or preservation of stationary pose. II. Adjustable parameters in muscles , 1966 .

[122]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[123]  E. Evarts.  RELATION OF DISCHARGE FREQUENCY TO CONDUCTION VELOCITY IN PYRAMIDAL TRACT NEURONS. , 1965, Journal of neurophysiology.

[124]  A. Craig,et al.  Retrograde analyses of spinothalamic projections in the macaque monkey: Input to ventral posterior nuclei , 2006, The Journal of comparative neurology.

[125]  J. Kaas.  The Evolution of the Dorsal Thalamus in Mammals , 2007 .

[126]  P. Snow,et al.  Cutaneous receptive field organization in the ventral posterior nucleus of the thalamus in the common marmoset. , 1999, Journal of neurophysiology.

[127]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during spiral tracing. , 1999, Journal of neurophysiology.

[128]  Alexa Riehle,et al.  Are extent and force independent movement parameters? Preparation- and movement-related neuronal activity in the monkey cortex , 2004, Experimental Brain Research.

[129]  John F Kalaska,et al.  Parietal area 5 activity does not reflect the differential time-course of motor output kinetics during arm-reaching and isometric-force tasks. , 2006, Journal of neurophysiology.

[130]  S. Scott,et al.  Reaching movements with similar hand paths but different arm orientations. II. Activity of individual cells in dorsal premotor cortex and parietal area 5. , 1997, Journal of neurophysiology.

[131]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during lemniscate tracing. , 1999, Journal of neurophysiology.

[132]  M. Bushnell,et al.  A thalamic nucleus specific for pain and temperature sensation , 1994, Nature.

[133]  H. Schaible,et al.  Joint receptors and kinaesthesia , 2004, Experimental Brain Research.

[134]  E. Evarts,et al.  Relation of pyramidal tract activity to force exerted during voluntary movement. , 1968, Journal of neurophysiology.

[135]  Christopher A. Buneo,et al.  Direct visuomotor transformations for reaching , 2002, Nature.

[136]  W. Wheeler,et al.  Dissociation between hand motion and population vectors from neural activity in motor cortex , 2022 .

[137]  S Grossberg,et al.  Kinematic coordinates in which motor cortical cells encode movement direction. , 2000, Journal of neurophysiology.