Review
Central processes for the multiparametric control of arm movements in primates

https://doi.org/10.1016/S0959-4388(01)00269-0Get rights and content

Abstract

Recent single-unit recording studies have clarified how multiple parameters of movement are signaled by individual cortical and cerebellar neurons, and also that multiple coordinate frames are utilized. Cognitive processes also modulate the firing of these neurons. The various signals and coordinate systems vary in time and evolve throughout a behavioral sequence, consistent with the demands of the task and the required sensorimotor transformations.

Introduction

Almost 20 years ago, the paradigm of correlating primary motor cortical neuronal firing to movements about an isolated joint [1] changed to correlating neuronal firing to whole arm movements [2]. This experimental shift was paralleled by a conceptual shift. The correlations once sought between neurons and parameters of muscle activity or single-joint movements 3., 4. were now sought between neurons and parameters of the hand trajectory 2., 5.. The focus turned to whether global or executive features of movement were encoded [6]. The debates intensified as to whether movements/kinematics or muscles/dynamics were controlled 7., 8., 9••.. Moreover, questions concerning the coordinate system in use became prominent. Neuronal correlates to joint or muscle parameters imply the use of an intrinsic (relative to the arm) coordinate system. Correlations to hand position or path in space imply an extrinsic coordinate system 8., 10., 11..

This paradigm shift added an experimental richness not possible for single joint movements. Yet the debate remained largely focused on elucidating the one crucial parameter of movement encoded or the one crucial coordinate system used in a motor area. In contradistinction, this review examines the central processing of motor signals during multi-joint limb movements and emphasizes four points.

First, the search for a single, dominant, encoded movement parameter is unlikely to be fruitful. All available evidence suggests that neurons in motor structures signal many aspects of limb movements and are modulated by various motor and non-motor factors. Second, the correlations with specific motor parameters are unlikely to be invariant but rather change in time or over a behavioral sequence as required by the task. Third, the search for a single coordinate frame in which a neuron encodes these parameters is also unlikely to be fruitful. Processing motor, sensory and cognitive parameters will involve information represented in several coordinate systems. These coordinate systems are thought to evolve sequentially during the sensorimotor transformations occurring with limb movements 12., 13., 14., 15.. Last, the parameters represented in the discharge of neurons reflect the tasks and paradigms being investigated. Task-specific processing may provide the flexibility needed to generate the vast repertoire of movements that human and non-human primates exhibit.

Section snippets

Directional tuning

Pivotal to the shift in the framework for studying the central control of arm movements was the observation by Georgopoulos et al. 2., 5. that the discharge of primary motor cortex (M1) neurons is broadly ‘tuned’ to the direction of arm movement for reaching in two and three dimensions. Characterization of the directional tuning typically includes fitting firing to a cosine-tuning function to define the preferred direction (PD) at which the firing is greatest. Directional tuning is a prominent

Encoding scalar parameters of arm movement

Accurate arm movements require the control of not only direction of movement but also other scalar parameters including speed, amplitude and accuracy. Human psychophysics point to the independent or serial processing of direction as well as other movement parameters 12., 41., 42., 43., 44., 45., 46.. Not surprisingly several non-directional scalars including amplitude 31., 47., 48., 49••., speed 9••., 16., 19., 22., 32. and accuracy [29•] also modulate the discharge of motor cortical and/or

Encoding other directionally sensitive parameters of arm movement

When neurons in the PMd and M1 signal both direction and a scalar, the directional tuning is not altered. The directional tuning of PMd and M1 neurons changes over time and during a behavioral sequence, consistent with the encoding of multiple directional parameters or vectors. In PMd and M1, the PD is influenced by arm posture 51., 52., 53. and starting position [54]. Eye position can shift the PD of these neurons 55., 56., as can visual target location 14., 15., 57. and selective attention

Coordinate systems and transforms

Whether intrinsic (e.g. joint angles or muscles) or extrinsic (e.g. hand- or workplace-centered) coordinate systems are used by M1 has been extensively debated 7., 8., 10., 40.. Because motor cortical neurons signal kinematic, dynamic, postural, visual and oculomotor information, the neural substrate exists for representing signals in multiple coordinate systems. Altering the required pronation–supination (forearm rotation) and flexion–extension movements of the wrist to move a cursor to a

Higher cortical processes also modulate PMd and M1 neurons

The relations of motor cortical neuronal firing to arm movements are not rigid; they depend not only on task-specific behavioral but also cognitive content 57., 67.. The changes in PD that occur with learning to move in a force field [60••], or with altered visuomotor relationships, illustrate how complex coordinate transformation alters the directional signal. Other higher cortical processes modulate motor cortical neuronal activity. The rotation of the PD of individual cells and the

Conclusions

The firing of PMd, M1 and cerebellar neurons contain many motor and non-motor signals. The most studied of these, directional tuning, is a robust phenomenon that has proved useful not only for understanding the planning and execution of movements but also for evaluating occult cognitive processing. But there is no single directional signal; instead, directional kinematic and kinetic variables contribute to the directional tuning. Within a behavioral context, the directional signal may vary in

Acknowledgements

The work was supported in part by NIH grants 5R01-NS31530 and 2R01-NS18338, and NSF grant IBN-9873478.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • •of special interest

  • ••of outstanding interest

References (75)

  • A.B. Schwartz et al.

    Primate motor cortex and free arm movements to visual targets in three-dimensional space. I. Relations between single cell discharge and direction of movement

    J Neurosci

    (1988)
  • A.P. Georgopoulos

    Higher order motor control

    Annu Rev Neurosci

    (1991)
  • S.H. Scott

    Role of motor cortex in coordinating multi-joint movements: is it time for a new paradigm?

    Can J Physiol Pharmacol

    (2000)
  • G.A. Reina et al.

    On the relationship between joint angular velocity and motor cortical discharge during reaching

    J Neurophysiol

    (2001)
  • J.F. Soechting et al.

    Moving in three-dimensional space: frames of reference, vectors and coordinate systems

    Annu Rev Neurosci

    (1992)
  • J.F. Kalaska et al.

    Cerebral cortical mechanisms of reaching movements

    Science

    (1992)
  • J.F. Soechting et al.

    Sensorimotor representations for pointing to targets in three-dimensional space

    J Neurophysiol

    (1989)
  • J. McIntyre et al.

    Analysis of pointing errors reveals properties of data representations and coordinate transformations within the central nervous system

    Neural Comput

    (2000)
  • L. Shen et al.

    Neural correlates of a spatial sensory-to-motor transformation in primary motor cortex

    J Neurophysiol

    (1997)
  • L. Shen et al.

    Preferential representation of instructed target location versus limb trajectory in dorsal premotor area

    J Neurophysiol

    (1997)
  • A.B. Schwartz

    Motor cortical activity during drawing movements: single-unit activity during sinusoid tracing

    J Neurophysiol

    (1992)
  • A.B. Schwartz et al.

    Motor cortical activity during drawing movements: population representation during lemniscate tracing

    J Neurophysiol

    (1999)
  • D.W. Moran et al.

    Motor cortical representation of speed and direction during reaching

    J Neurophysiol

    (1999)
  • D.W. Moran et al.

    Motor cortical activity during drawing movements: population representation during spiral tracing

    J Neurophysiol

    (1999)
  • M.T.V. Johnson et al.

    Encoding of target direction and speed during visual instruction and arm tracking in dorsal premotor and primary motor cortical neurons

    Eur J Neurosci

    (1999)
  • M.T.V. Johnson et al.

    Visuomotor processing as reflected in the directional discharge of premotor and primary motor cortex neurons

    J Neurophysiol

    (1999)
  • N.L. Port et al.

    Motor cortical activity during interception of moving targets

    J Cogn Neurosci

    (2001)
  • A.P. Georgopoulos et al.

    The motor cortex and the coding of force

    Science

    (1992)
  • M. Taira et al.

    On the relations between single cell activity in the motor cortex and the direction and magnitude of three-dimensional static isometric force

    Exp Brain Res

    (1996)
  • L.E. Sergio 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

    J Neurophysiol

    (1997)
  • L.E. Sergio et al.

    Changes in the temporal pattern of primary motor cortex activity in a directional isometric force versus limb movement task

    J Neurophysiol

    (1998)
  • D.J. Crammond et al.

    Modulation of preparatory neuronal activity in dorsal premotor cortex due to stimulus-response compatibility

    J Neurophysiol

    (1994)
  • J.E. Gomez et al.

    Representation of accuracy in the dorsal premotor cortex

    Eur J Neurosci

    (2000)
  • P.A. Fortier et al.

    Cerebellar neuronal activity related to whole-arm reaching movements in the monkey

    J Neurophysiol

    (1989)
  • Q.G. Fu et al.

    Relationship of cerebellar Purkinje cell simple spike discharge to movement kinematics in the monkey

    J Neurophysiol

    (1997)
  • J.D. Coltz et al.

    Cerebellar Purkinje cell simple spike discharge encodes movement velocity in primates during visuomotor arm tracking

    J Neurosci

    (1999)
  • D.A. Cohen et al.

    Tactile activity in primate primary somatosensory cortex during active arm movements: correlation with receptive field properties

    J Neurophysiol

    (1994)
  • Cited by (37)

    • Activity in Primary Motor Cortex Related to Visual Feedback

      2019, Cell Reports
      Citation Excerpt :

      The concept of smoothly evolving lawful neuronal dynamics, although appealing, may simply reflect the smooth changes characteristic of movement kinematics (Flash and Hogan, 1985). A “temporal parcellation scheme” may constitute a useful compromise between these two descriptions of M1 activity (Johnson et al., 2001). Much like the “dynamical systems” perspective, this scheme predicts that firing rates covary with task-related parameters in a time-varying sequence (Shenoy et al., 2013).

    • The influence of target sensory modality on motor planning may reflect errors in sensori-motor transformations

      2009, Neuroscience
      Citation Excerpt :

      Sensory signals from different modalities are likely represented in different coordinate systems, reflecting the characteristics of the sensory channels. It thus appears that multi-sensory integration for motor planning requires neural computations akin to coordinate transformations (Johnson et al., 2001; Kakei et al., 2001). Currently, visually-targeted movements are thought to be planned in visual coordinates (Flanagan and Rao, 1995; Wolpert et al., 1995; Buneo et al., 2002), based on the visually-defined starting hand and target positions (Sainburg et al., 2003; Sober and Sabes, 2005).

    View all citing articles on Scopus
    View full text