Timing of bimanual movements in human and non-human primates in relation to neuronal activity in primary motor cortex and supplementary motor area

This study investigates the timing of bimanual movements in a combined behavioral and physiological approach. Human subjects and rhesus monkeys performed the same bimanual task. In monkeys, we simultaneously recorded neuronal activity in the two hemispheres of primary motor cortex (MI) or supplementary motor area (SMA), and related it to bimanual coordination in the temporal domain. Both for monkeys and humans, the reaction times of bimanual movements never significantly exceeded the reaction times of the slower arm in unimanual movements. Consistent with this, the longest delay between neural activity onset in SMA and MI and movement initiation was observed in unimanual movements of the slower arm and not in bimanual movements. Both results suggest that the programming of bimanual movements does not require more processing time than unimanual movements. They are also consistent with the view that bimanual movements are programmed in a single process, rather than by combining two separate unimanual movement plans. In both humans and monkeys, movement initiation was highly correlated between the arms. However, once movements began, the temporal correlation between the arms progressively declined. Movement decorrelation was accompanied by a net decorrelation of neuronal population activity in MI and SMA, suggesting a functional connection between neuronal interactions and the level of bimanual coupling and decoupling. The similarity of neuronal activities in MI and SMA in relationship to behavioral timing lends support to the idea that both areas are involved in the temporal coordination of the arms.

[1]  Bernice W. Polemis Nonparametric Statistics for the Behavioral Sciences , 1959 .

[2]  N. A. Bernshteĭn The co-ordination and regulation of movements , 1967 .

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

[4]  B. Preilowski,et al.  Possible contribution of the anterior forebrain commissures to bilateral motor coordination. , 1972, Neuropsychologia.

[5]  Easton Ta On the normal use of reflexes. , 1972 .

[6]  E V Evarts,et al.  Precentral and postcentral cortical activity in association with visually triggered movement. , 1974, Journal of neurophysiology.

[7]  B. Preilowski,et al.  Bilateral Motor Interaction: Perceptual-Motor Performance of Partial and Complete “Split-Brain” Patients , 1975 .

[8]  R. Schmidt A schema theory of discrete motor skill learning. , 1975 .

[9]  P H Ellaway An application of cumulative sum technique (cusums) to neurophysiology [proceedings]. , 1977, The Journal of physiology.

[10]  D Goodman,et al.  On the coordination of two-handed movements. , 1979, Journal of experimental psychology. Human perception and performance.

[11]  H. Zelaznik,et al.  Motor-output variability: a theory for the accuracy of rapid motor acts. , 1979, Psychological review.

[12]  C. Brinkman Supplementary motor area of the monkey's cerebral cortex: short- and long-term deficits after unilateral ablation and the effects of subsequent callosal section , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  C. MacKenzie,et al.  Bimanual Movement Control: Information processing and Interaction Effects , 1984 .

[14]  H. Kornhuber,et al.  Timing function of the frontal cortex in sequential motor and learning tasks. , 1985, Human neurobiology.

[15]  G. Goldberg Supplementary motor area structure and function: Review and hypotheses , 1985, Behavioral and Brain Sciences.

[16]  R. Stein,et al.  Statistical limits for detecting change in the cumulative sum derivative of the peristimulus time histogram , 1986, Journal of Neuroscience Methods.

[17]  C. MacKenzie,et al.  Three-Dimensional Movement Trajectories in Fitts' Task: Implications for Control , 1987 .

[18]  J. Tanji,et al.  Relation of neurons in the nonprimary motor cortex to bilateral hand movement , 1987, Nature.

[19]  J. Tanji,et al.  Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. , 1988, Journal of neurophysiology.

[20]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.

[21]  T. Milner,et al.  The effect of accuracy constraints on three-dimensional movement kinematics , 1990, Neuroscience.

[22]  B. Fowler,et al.  The Coordination of Bimanual Aiming Movements: Evidence for Progressive Desynchronization , 1991, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[23]  B. Hyland,et al.  Comparison of neural activity in the supplementary motor area and in the primary motor cortex in monkeys. , 1991, Somatosensory & motor research.

[24]  H. Lüders,et al.  Movement-related potentials recorded from supplementary motor area and primary motor area. Role of supplementary motor area in voluntary movements. , 1992, Brain : a journal of neurology.

[25]  J. Greg Anson,et al.  Neuromotor programming: Bilateral and unilateral effects on simple reaction time , 1993 .

[26]  M. A. Arbib,et al.  Models of Trajectory Formation and Temporal Interaction of Reach and Grasp. , 1993, Journal of motor behavior.

[27]  A. Riehle,et al.  The predictive value for performance speed of preparatory changes in neuronal activity of the monkey motor and premotor cortex , 1993, Behavioural Brain Research.

[28]  M. Wiesendanger,et al.  Temporal Structure of a Bimanual Goal‐directed Movement Sequence in Monkeys , 1994, The European journal of neuroscience.

[29]  I Rektor,et al.  Intracerebral recording of movement related readiness potentials: an exploration in epileptic patients. , 1994, Electroencephalography and clinical neurophysiology.

[30]  J Tanji,et al.  Corticocortical and thalamocortical responses of neurons in the monkey primary motor cortex and their relation to a trained motor task. , 1994, Journal of neurophysiology.

[31]  M. Gazzaniga,et al.  Dissociation of Spatial and Temporal Coupling in the Bimanual Movements of Callosotomy Patients , 1996 .

[32]  I. Kermadi,et al.  Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination. , 1998, Somatosensory & motor research.

[33]  E. Vaadia,et al.  Primary motor cortex is involved in bimanual coordination , 1998, Nature.

[34]  Will Spijkers,et al.  The time course of cross-talk during the simultaneous specification of bimanual movement amplitudes , 1998, Experimental Brain Research.

[35]  Casper J. Erkelens,et al.  Variability and correlations in bi-manual pointing movements , 1999 .

[36]  K. Zilles,et al.  The role of ventral medial wall motor areas in bimanual co-ordination. A combined lesion and activation study. , 1999, Brain : a journal of neurology.

[37]  B. Hyland,et al.  Neural activity of supplementary and primary motor areas in monkeys and its relation to bimanual and unimanual movement sequences , 1999, Neuroscience.

[38]  Michael S. Gazzaniga,et al.  Direction information coordinated via the posterior third of the corpus callosum during bimanual movements , 1999, Experimental Brain Research.

[39]  Ian M. Franks,et al.  Reaction time differences in spatially constrained bilateral and unilateral movements , 2000, Experimental Brain Research.

[40]  I. Kermadi,et al.  Do bimanual motor actions involve the dorsal premotor (PMd), cingulate (CMA) and posterior parietal (PPC) cortices? Comparison with primary and supplementary motor cortical areas. , 2000, Somatosensory & motor research.

[41]  M. Himmelbach,et al.  fMRI study of bimanual coordination , 2000, Neuropsychologia.

[42]  M S Gazzaniga,et al.  Anterior and posterior callosal contributions to simultaneous bimanual movements of the hands and fingers. , 2000, Brain : a journal of neurology.

[43]  Scott T. Grafton,et al.  Forward modeling allows feedback control for fast reaching movements , 2000, Trends in Cognitive Sciences.

[44]  Borís Burle,et al.  Deficit in motor cortical activity for simultaneous bimanual responses , 2001, Experimental Brain Research.

[45]  E. Vaadia,et al.  Neural interactions between motor cortical hemispheres during bimanual and unimanual arm movements , 2001, The European journal of neuroscience.

[46]  Will Spijkers,et al.  Static and Phasic Cross-Talk Effects in Discrete Bimanual Reversal Movements , 2001, Journal of motor behavior.

[47]  O. Donchin,et al.  Local field potentials related to bimanual movements in the primary and supplementary motor cortices , 2001, Experimental Brain Research.

[48]  A. Morel,et al.  Neuronal activity in primate striatum and pallidum related to bimanual motor actions , 2002, Neuroreport.

[49]  O. Donchin,et al.  Neuronal populations in primary motor cortex encode bimanual arm movements , 2002, The European journal of neuroscience.

[50]  G. Tassinari,et al.  Hemispheric control of unilateral and bilateral responses to lateralized light stimuli after callosotomy and in callosal agenesis , 2004, Experimental Brain Research.

[51]  J. Kelso,et al.  Environmentally-specified patterns of movement coordination in normal and split-brain subjects , 2004, Experimental Brain Research.

[52]  M. Hallett,et al.  Cortical motor representation of the ipsilateral hand and arm , 2004, Experimental Brain Research.

[53]  C. A. Marzi,et al.  Hemispheric control of unilateral and bilateral movements of proximal and distal parts of the arm as inferred from simple reaction time to lateralized light stimuli in man , 2004, Experimental Brain Research.

[54]  M. Wiesendanger,et al.  Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys , 2004, Experimental Brain Research.