Motor subcircuits mediating the control of movement velocity: a PET study.

The influence of changes in the mean velocity of movement on regional cerebral blood flow (rCBF) was studied using positron emission tomography (PET) in nine healthy right-handed adults while they performed a smooth pursuit visuomanual tracking task. Images of relative rCBF were obtained while subjects moved a hand-held joystick to track the movement of a target at three different rates of a sinusoidal displacement (0.1, 0.4, and 0.7 Hz). Significant changes in rCBF between task conditions were detected using analysis of variance and weighted linear contrasts. The kinematics of arm and eye movements indicated that subjects performed tasks in a similar manner, particularly during the faster two tracking conditions. Significant increases in rCBF during arm movement (relative to an eye tracking only control condition) were detected in a widespread network of areas known for their involvement in motor control. The activated areas included primary sensorimotor (M1S1), dorsal and mesial premotor, and dorsal parietal cortices in the left hemisphere and to a lesser extent the sensorimotor and superior parietal cortices in the right hemisphere. Subcortically, activations were found in the left putamen, globus pallidus (GP), and thalamus, in the right basal ganglia, and in the right anterior cerebellum. Within the cerebral volume activated with movement, three areas had changes in rCBF that correlated positively with the rate of movement: left M1S1, left GP, and right anterior cerebellum. No movement-related sites had rCBF that correlated negatively with the rate of movement. Regressions of mean percent change (MPC) in rCBF onto mean hand velocity yielded two nonoverlapping subpopulations of movement-related loci, the three sites with significant rate effects and regression slopes steeper than 0.17 MPC.cm-1.s-1 and all other sites with nonsignificant rate effects and regression slopes below 0.1 MPC.cm-1. s-1. Moreover, the effects of movement per se and of movement velocity varied in magnitude independently. These results confirm previous reports that movement-related activations of M1S1 and cerebellum are sensitive to movement frequency or some covarying parameter of movement. The activation of GP with increasing movement velocity, not described in previous functional-imaging studies, supports the hypothesis that the basal ganglia motor circuit may be involved preferentially in controlling or monitoring the scale and/or dynamics of arm movements. The remaining areas that were activated equally for all movement rates may be involved in controlling higher level aspects of motor control that are independent of movement dynamics.

[1]  J. V. Blachford The Functions of the Basal Ganglia , 1922 .

[2]  P. Fitts The information capacity of the human motor system in controlling the amplitude of movement. , 1954, Journal of experimental psychology.

[3]  F. Plum Handbook of Physiology. , 1960 .

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

[5]  A L Towe,et al.  Extracellular microelectrode sampling bias. , 1970, Experimental neurology.

[6]  Michael H. Kutner Applied Linear Statistical Models , 1974 .

[7]  G. Schaltenbrand,et al.  Atlas for Stereotaxy of the Human Brain , 1977 .

[8]  M. Hepp-Reymond,et al.  Neuronal coding of static force in the primate motor cortex. , 1978, Journal de physiologie.

[9]  J. Murphy,et al.  Spatial organization of precentral cortex in awake primates. III. Input-output coupling. , 1978, Journal of neurophysiology.

[10]  Allan M. Smith The activity of supplementary motor area neurons during a maintained precision grip , 1979, Brain Research.

[11]  E. Fetz,et al.  Sensory and motor responses of precentral cortex cells during comparable passive and active joint movements. , 1980, Journal of neurophysiology.

[12]  M. Hallett,et al.  A physiological mechanism of bradykinesia. , 1980, Brain : a journal of neurology.

[13]  P. Roland,et al.  Supplementary motor area and other cortical areas in organization of voluntary movements in man. , 1980, Journal of neurophysiology.

[14]  N. Mano,et al.  Simple-spike activity of cerebellar Purkinje cells related to visually guided wrist tracking movement in the monkey. , 1980, Journal of neurophysiology.

[15]  C. K. Yuen,et al.  Digital Filters , 1979, IEEE Transactions on Systems, Man, and Cybernetics.

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

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

[18]  Edward V. Evarts,et al.  Pyramidal tract neurons in somatosensory cortex: central and peripheral inputs during voluntary movement , 1982, Brain Research.

[19]  P. Viviani,et al.  Trajectory determines movement dynamics , 1982, Neuroscience.

[20]  S. Wise,et al.  The premotor cortex of the monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  Michel Bonnet,et al.  Specification of direction and extent in motor programming , 1982 .

[22]  J Tanji,et al.  Comparison of movement-related activity in two cortical motor areas of primates. , 1982, Journal of neurophysiology.

[23]  V. A. Jennings,et al.  Somatosensory cortex activity related to position and force. , 1983, Journal of neurophysiology.

[24]  M. D. Crutcher,et al.  Relations between parameters of step-tracking movements and single cell discharge in the globus pallidus and subthalamic nucleus of the behaving monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  C. Fromm,et al.  Contrasting properties of pyramidal tract neurons located in the precentral or postcentral areas and of corticorubral neurons in the behaving monkey. , 1983, Advances in neurology.

[26]  M. Raichle,et al.  Brain blood flow measured with intravenous H2(15)O. I. Theory and error analysis. , 1983, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[27]  M. Mintun,et al.  Brain blood flow measured with intravenous H2(15)O. II. Implementation and validation. , 1983, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[28]  J. Brodzinski Three-way analysis of variance , 1983 .

[29]  P. Roland Organization of motor control by the normal human brain. , 1984, Human neurobiology.

[30]  F. Horak,et al.  Influence of globus pallidus on arm movements in monkeys. II. Effects of stimulation. , 1984, Journal of neurophysiology.

[31]  Arthur Prochazka,et al.  Methods for neuronal recording in conscious animals , 1984 .

[32]  F. Horak,et al.  Influence of globus pallidus on arm movements in monkeys. I. Effects of kainic acid-induced lesions. , 1984, Journal of neurophysiology.

[33]  J. Mazziotta,et al.  A Noninvasive Positron Computed Tomography Technique Using Oxygen-15-Labeled Water for the Evaluation of Neurobehavioral Task Batteries , 1985, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[34]  M. D. Crutcher,et al.  Primate globus pallidus and subthalamic nucleus: functional organization. , 1985, Journal of neurophysiology.

[35]  J. Tanji,et al.  Contrasting neuronal activity in supplementary and precentral motor cortex of monkeys. I. Responses to instructions determining motor responses to forthcoming signals of different modalities. , 1985, Journal of neurophysiology.

[36]  G. Rizzolatti,et al.  Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey , 1985, Behavioural Brain Research.

[37]  S. L. Liles Activity of neurons in putamen during active and passive movements of wrist. , 1985, Journal of neurophysiology.

[38]  Marie-Claude Hepp-Reymond,et al.  Neuronal activity in the postcentral cortex related to force regulation during a precision grip task , 1986, Brain Research.

[39]  André Parent,et al.  Comparative neurobiology of the basal ganglia , 1986 .

[40]  R. Miall,et al.  Manual tracking of visual targets by trained monkeys , 1986, Behavioural Brain Research.

[41]  P. Thompson,et al.  The coexistence of bradykinesia and chorea in Huntington's disease and its implications for theories of basal ganglia control of movement. , 1988, Brain : a journal of neurology.

[42]  J Hore,et al.  Relations of motor cortex neural discharge to kinematics of passive and active elbow movements in the monkey. , 1988, Journal of neurophysiology.

[43]  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.

[44]  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.

[45]  M Corbetta,et al.  Attentional modulation of neural processing of shape, color, and velocity in humans. , 1990, Science.

[46]  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.

[47]  G. E. Alexander,et al.  Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. , 1990, Progress in brain research.

[48]  M. Inase,et al.  Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. , 1991, Journal of neurophysiology.

[49]  J C Mazziotta,et al.  Somatotopic mapping of the primary motor cortex in humans: activation studies with cerebral blood flow and positron emission tomography. , 1991, Journal of neurophysiology.

[50]  G. Rizzolatti,et al.  Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey , 1991, The Journal of comparative neurology.

[51]  Karl J. Friston,et al.  Regional cerebral blood flow during voluntary arm and hand movements in human subjects. , 1991, Journal of neurophysiology.

[52]  W T Thach,et al.  Basal ganglia motor control. III. Pallidal ablation: normal reaction time, muscle cocontraction, and slow movement. , 1991, Journal of neurophysiology.

[53]  W. T. Thach,et al.  Basal ganglia motor control. II. Late pallidal timing relative to movement onset and inconsistent pallidal coding of movement parameters. , 1991, Journal of neurophysiology.

[54]  P. Brotchie,et al.  Motor function of the monkey globus pallidus. 1. Neuronal discharge and parameters of movement. , 1991, Brain : a journal of neurology.

[55]  M. Taussig The Nervous System , 1991 .

[56]  D. Burke,et al.  Does the nervous system depend on kinesthetic information to control natural limb movements , 1992 .

[57]  E. Fetz Movement control: Are movement parameters recognizably coded in the activity of single neurons? , 1992 .

[58]  M. Hariz,et al.  Leksell's posteroventral pallidotomy in the treatment of Parkinson's disease. , 1992, Journal of neurosurgery.

[59]  J Jacquy,et al.  Parkinsonian bradykinesia is due to depression in the rate of rise of muscle activity , 1992, Annals of neurology.

[60]  M. Kimura,et al.  Effects of reversible blockade of basal ganglia on a voluntary arm movement. , 1992, Journal of neurophysiology.

[61]  J. F. Soechting,et al.  Early stages in a sensorimotor transformation , 1992, Behavioral and Brain Sciences.

[62]  Simon C. Gandevia,et al.  Kinesthesia and unique solutions for control of multijoint movements , 1992, Behavioral and Brain Sciences.

[63]  H J Sagar,et al.  A component analysis of the generation and release of isometric force in Parkinson's disease. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[64]  J. Houk,et al.  Movement-related inputs to intermediate cerebellum of the monkey. , 1993, Journal of neurophysiology.

[65]  P. Strick,et al.  Preferential activity of dentate neurons during limb movements guided by vision. , 1993, Journal of neurophysiology.

[66]  J. Mazziotta,et al.  Automated image registration , 1993 .

[67]  T. Ebner,et al.  Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. , 1993, Journal of neurophysiology.

[68]  K. Kurata,et al.  Premotor cortex of monkeys: set- and movement-related activity reflecting amplitude and direction of wrist movements. , 1993, Journal of neurophysiology.

[69]  R. Passingham The frontal lobes and voluntary action , 1993 .

[70]  U Sabatini,et al.  Journal of Cerebral Blood Flow and Metabolism Effect of Side and Rate of Stimulation on Cerebral Blood Flow Changes in Motor Areas during Finger Movements in Humans , 2022 .

[71]  A. P. Georgopoulos,et al.  Movement parameters and neural activity in motor cortex and area 5. , 1994, Cerebral cortex.

[72]  Scott T. Grafton,et al.  Parceling of mesial frontal motor areas during ideation and movement using functional magnetic resonance imaging at 1.5 tesla , 1994, Annals of neurology.

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

[74]  Y. Samson,et al.  Movement‐ and task‐related activations of motor cortical areas: A positron emission tomographic study , 1994, Annals of neurology.

[75]  M. Hepp-Reymond,et al.  Force-related neuronal activity in two regions of the primate ventral premotor cortex. , 1994, Canadian journal of physiology and pharmacology.

[76]  S G Lisberger,et al.  Simple spike responses of gaze velocity Purkinje cells in the floccular lobe of the monkey during the onset and offset of pursuit eye movements. , 1994, Journal of neurophysiology.

[77]  P. Strick,et al.  Activation of a cerebellar output nucleus during cognitive processing. , 1994, Science.

[78]  C. Marsden,et al.  The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson's disease. , 1994, Brain : a journal of neurology.

[79]  J. Mazziotta,et al.  Mapping motor representations with positron emission tomography , 1994, Nature.

[80]  M. Jüptner,et al.  Review: Does Measurement of Regional Cerebral Blood Flow Reflect Synaptic Activity?—Implications for PET and fMRI , 1995, NeuroImage.

[81]  Remo Guidieri Res , 1995, RES: Anthropology and Aesthetics.

[82]  O. Devinsky,et al.  Stereotactic ventral pallidotomy for Parkinson's disease , 1995, Neurology.

[83]  R. Passingham,et al.  Relation between cerebral activity and force in the motor areas of the human brain. , 1995, Journal of neurophysiology.

[84]  M. Hallett,et al.  Velocity sensitivity of human muscle spindle afferents and slowly adapting type II cutaneous mechanoreceptors. , 1995, The Journal of physiology.

[85]  A. Georgopoulos Current issues in directional motor control , 1995, Trends in Neurosciences.

[86]  W. T. Thach,et al.  Cerebellar outflow lesions: A comparison of movement deficits resulting from lesions at the levels of the cerebellum and thalamus , 1995, Annals of neurology.

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

[88]  M. Hallett,et al.  Regional cerebral blood flow changes in motor cortical areas after transient anesthesia of the forearm , 1995, Annals of neurology.

[89]  R. Passingham,et al.  Functional anatomy of the mental representation of upper extremity movements in healthy subjects. , 1995, Journal of neurophysiology.

[90]  M. Jüptner,et al.  Localization of a cerebellar timing process using PET , 1995, Neurology.

[91]  J. W. VanMeter,et al.  Parametric Analysis of Functional Neuroimages: Application to a Variable-Rate Motor Task , 1995, NeuroImage.

[92]  Stefan Knecht,et al.  Altered force release control in Parkinson's disease , 1995, Behavioural Brain Research.

[93]  M. Alamy,et al.  A defective control of small-amplitude movements in monkeys with globus pallidus lesions: an experimental study on one component of pallidal bradykinesia , 1995, Behavioural Brain Research.

[94]  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.

[95]  T. Ebner,et al.  Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. , 1995, Journal of neurophysiology.

[96]  C. Svarer,et al.  Rate Dependence of Regional Cerebral Activation during Performance of a Repetitive Motor Task: A PET Study , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[97]  W. T. Thach,et al.  Cerebellar ataxia: abnormal control of interaction torques across multiple joints. , 1996, Journal of neurophysiology.

[98]  Richard S. J. Frackowiak,et al.  Cerebral activation during the exertion of sustained static force in man , 1996, Neuroreport.

[99]  M. Hallett,et al.  Cerebral structures participating in motor preparation in humans: a positron emission tomography study. , 1996, Journal of neurophysiology.

[100]  Scott T. Grafton,et al.  Functional anatomy of pointing and grasping in humans. , 1996, Cerebral cortex.

[101]  Karl J. Friston,et al.  Quantitative Comparison of Functional Magnetic Resonance Imaging with Positron Emission Tomography Using a Force-Related Paradigm , 1996, NeuroImage.

[102]  G. Schlaug,et al.  Cerebral activation covaries with movement rate , 1996, Neuroreport.

[103]  A. Cools,et al.  Movement preparation in Parkinson's disease. Time course and distribution of movement-related potentials in a movement precueing task. , 1996, Brain : a journal of neurology.

[104]  P A Bandettini,et al.  Relationship between Finger Movement Rate and Functional Magnetic Resonance Signal Change in Human Primary Motor Cortex , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[105]  K. Zilles,et al.  Functions and structures of the motor cortices in humans , 1996, Current Opinion in Neurobiology.

[106]  M. E. Anderson,et al.  Changes in the control of arm position, movement, and thalamic discharge during local inactivation in the globus pallidus of the monkey. , 1996, Journal of neurophysiology.

[107]  T. Paus Location and function of the human frontal eye-field: A selective review , 1996, Neuropsychologia.

[108]  J. Mazziotta,et al.  Brain-behavior relationships: evidence from practice effects in spatial stimulus-response compatibility. , 1996, Journal of neurophysiology.

[109]  C Ghez,et al.  Learning of scaling factors and reference axes for reaching movements. , 1996, Neuroreport.

[110]  M. Hallett,et al.  Frequency-Dependent Changes of Regional Cerebral Blood Flow during Finger Movements , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[111]  R. Turner,et al.  Treatment of advanced Parkinson's disease by posterior GPi pallidotomy: 1‐year results of a pilot study , 1996, Annals of neurology.

[112]  Paul B. Johnson,et al.  Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. , 1996, Cerebral cortex.

[113]  M. Hallett,et al.  Single-joint rapid arm movements in normal subjects and in patients with motor disorders. , 1996, Brain : a journal of neurology.

[114]  Richard S. J. Frackowiak,et al.  Multiple nonprimary motor areas in the human cortex. , 1997, Journal of neurophysiology.

[115]  M. E. Anderson,et al.  Pallidal discharge related to the kinematics of reaching movements in two dimensions. , 1997, Journal of neurophysiology.

[116]  T. Ebner,et al.  Movement kinematics encoded in complex spike discharge of primate cerebellar Purkinje cells , 1997, Neuroreport.

[117]  R Verleger,et al.  Responses to cued signals in Parkinson's disease. Distinguishing between disorders of cognition and of activation. , 1997, Brain : a journal of neurology.

[118]  Julie Messier,et al.  Differential effect of task conditions on errors of direction and extent of reaching movements , 1997, Experimental Brain Research.

[119]  R. Passingham,et al.  The effect of movement frequency on cerebral activation: a positron emission tomography study , 1997, Journal of the Neurological Sciences.

[120]  Scott T. Grafton,et al.  Premotor Cortex Activation during Observation and Naming of Familiar Tools , 1997, NeuroImage.

[121]  P. Skudlarski,et al.  An fMRI study of the human cortical motor system response to increasing functional demands. , 1997, Magnetic resonance imaging.

[122]  J. Bower,et al.  Is the cerebellum sensory for motor's sake, or motor for sensory's sake: the view from the whiskers of a rat? , 1997, Progress in brain research.

[123]  C. Ghez,et al.  Discrete and continuous planning of hand movements and isometric force trajectories , 1997, Experimental Brain Research.

[124]  M. Hallett,et al.  Frequency-Dependent Changes of Regional Cerebral Blood Flow during Finger Movements: Functional MRI Compared to PET , 1997, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[125]  T J Ebner,et al.  Relationship of cerebellar Purkinje cell simple spike discharge to movement kinematics in the monkey. , 1997, Journal of neurophysiology.

[126]  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.

[127]  G E Alexander,et al.  Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. , 1997, Journal of neurophysiology.

[128]  Scott T. Grafton,et al.  Motor task difficulty and brain activity: investigation of goal-directed reciprocal aiming using positron emission tomography. , 1997, Journal of neurophysiology.

[129]  T. Aird Functional Anatomy of the Basal Ganglia , 2000, The Journal of neuroscience nursing : journal of the American Association of Neuroscience Nurses.