Elsevier

Behavioural Brain Research

Volume 87, Issue 2, September 1997, Pages 255-269
Behavioural Brain Research

Erratum
Erratum to “Force and the motor cortex”: [Behavioural Brain Research 86 (1997) 1–15]1

https://doi.org/10.1016/S0166-4328(97)00752-3Get rights and content

Abstract

The Publisher regrets that this article was printed without incorporating several Author's Corrections. The corrected article is reprinted in the following pages.The relation between the activity of cells in the motor cortex and static force has been studied extensively. Most studies have concentrated on the relation to the magnitude of force; this relation is more or less monotonic. The slope of the relation, however, shows considerable variation among different studies and seems to be inversely associated with the range of forces over which the cell activity has been studied. Cells in the motor cortex also show variation in activity with the direction of static force. When both the direction and the magnitude of static force are allowed to vary, a majority of cells show significant changes in activity with direction of force alone, an intermediate number relate to both direction and magnitude, while a small number relate purely to the magnitude. This suggests that the direction of static force can be controlled independently of its magnitude and that this directional signal is especially prominent in the motor cortex. In general, it has been more difficult to study the relations to dynamic force. There is a correlation between motor cortex cell activity and the rate of change of force. The direction of dynamic force is also an important determinant of cell activity. When both static and dynamic force output are required (for example, with arm movement in the presence of gravity) it is the dynamic signal that is most clearly reflected in motor cortex activity. The relations between motor cortex activity and static or dynamic force are not invariant, but may be modified by the behavioral context of the motor output.

Introduction

The investigations into the relation between the parameters of movement and the activity of cells in the motor cortex were strongly influenced from the beginning by the work of Sherrington and his colleagues 32, 49. This work has been used to support the conception that there is a fixed relation between specific areas (or cells) in the motor cortex and the muscles involved in movement. Although Leyton and Sherrington [49]did refer to the “punctate localization” of muscles within the motor cortex, their experiments clearly documented a much more complex association between the cortex and muscles. Neither did they consider that the relation between the cortex and elements of the motor output was fixed, in fact, they state explicitly that “the motor cortex is a labile organ” (Ref. [49], p. 144). As regards function, they suggested that “the upbuilding of larger combinations (of movements) varied in character ... is one of the main offices performed by the motor cortex” (Ref. [49], p. 178). One of the conclusions in their paper is that the motor cortex performs an integrative function wherein whole movements are constructed, and does not subserve the control of single muscles. This is in keeping with the earlier suggestion of Hughlins Jackson that “muscles are represented in the nervous centres in thousands of different combinations – that is, as very many different movements” 42, 43. Nevertheless, later work continued to use what was assumed (erroneously) to be the imprimatur of Sherrington, in putting forward what were regarded as similar results [9]. Consequently, the idea that cells in the motor cortex are literally `upper motor neurons' has been the dominant one which has been tremendously influential in neurology and neurophysiology.

If one accepts the hypothesis that muscles are represented within the motor cortex then force is the most obvious motor parameter to study as force is generated by muscle activity. To imagine that the activity of cells could relate to another parameter, such as amplitude, velocity, or direction, assumes a more sophisticated relation between motor cortex and muscle than was generally allowed. Therefore, from the earliest motor behavioral experiments in the monkey, force was the parameter that has received most attention. Force is a vector, and as such, has both magnitude and direction. However, it is the magnitude of force, which could be related to the activity of a single muscle, rather than the direction that has been the main focus of research. There have been several recent developments in the study of force coding by the motor cortex that question previous views of the motor cortex as a controller of muscles and take us closer to Sherrington's concept of the function of the motor cortex as one of integration.

In addition to reviewing the work on force, we will attempt to outline how our current understanding of the way in which this variable is controlled is in keeping with changing attitudes to the role of the motor cortex in motor output. The review deals predominantly with experiments using the technique of single cell recording in awake behaving animals which gives fine grain information about the activity of cells in the intact organism.

Section snippets

Relations to magnitude of force under static conditions

Following the introduction of the technique of extracellular single cell recording in awake behaving animals in the late 1950s 39, 60, Evarts [13]was the first to usefully apply it to the study of motor function. Many of the experiments were done under static isometric (or semi-isometric) conditions; it was expected that these behavioral conditions would lead to the least ambiguous results concerning the motor cortical coding of the magnitude of static force. Recent work suggests that the

Relations to magnitude of force under dynamic conditions

The relations of cell activity to force under dynamic conditions (i.e., when the force is changing) have not been studied extensively. In addition, there have been numerous aspects of experimental design which have complicated the interpretation of data dealing with the control of dynamic force: actual forces were not measured, the behavioral tasks also involved movement, and the behavioral repertoire of the tasks was limited.

Evarts, in his original work, suggested that cell activity related to

Nature of the relation to force

The studies reviewed briefly above, raise a number of issues about the nature of the relation between neural activity and the magnitude of force.

Behavioral context of neural activity

The earliest comprehensive study of the behavioral context of neural activity examined the relation between isometric contraction in pairs of agonist/antagonist muscles in the arm and the activity of cells in the motor cortex [16]. Beginning with the premise that motor cortex activity and muscle activity were related in some general way, the authors sought to characterize this relation. Eight of ten cells examined changed activity during the contraction of more than one of the muscles. Only one

Directional aspects of static force

Force is a vector and as such has both direction and magnitude. The majority of studies on force and its relation to cell activity in the motor cortex have failed to take account of the directional nature of force. This is not to say that the direction of force output has not been a consideration in these studies, but that the experimental design was such that force was generally examined in one dimension only: for example, flexion and extension at the elbow [11]or the wrist 10, 72,

Directional aspects of dynamic force

The control of force output under two dimensional dynamic conditions has recently been specifically addressed [21]. A task was designed in which a monkey exerted dynamic force in two dimensions under isometric conditions. Constant bias forces were incorporated into the task which dissociated three force variables: the force exerted by the subject, the net force and the change in force. This dissociation of forces allowed for the simulation under isometric conditions of the situation that

Spinal interneuronal systems and force

In a series of experiments using a spinal frog preparation, Bizzi and colleagues 7, 31microstimulated the spinal gray matter while measuring forces produced at the ankle. The animal was immobilized, and the force transducer on the ankle functioned as a clamp, allowing isometric forces to be measured. The frog leg was positioned at various locations on a two-dimensional work-surface and the forces acting on the ankle were measured at each location during stimulation of a point within the spinal

Acknowledgements

This work was supported by a Merit Review grant from the United States Department of Veterans Affairs to J.A.

References (75)

  • Amos, A., Armstrong, D.M. and Marple-Horvat, D.E., Changes in the discharge patterns of cortical motor neurons...
  • Armstrong, D.M. and Drew, T., Discharges of pyramidal tract and other motor cortical neurones during locomotion in the...
  • Alstermack, B., Lindstrom, S., Lundberg, A. and Sybirska, E., Integration in descending motor pathways controlling the...
  • Bahill, A.T., Clark, M.R. and Stark, L., The main sequence, a tool for studying human eye movements, Math. Biosci., 24...
  • Beloozerova, I.N. and Sirota, M.G., Role of motor cortex in control of locomotion. In: V.S. Gurfinkel, M.E. Ioffe, J....
  • Bernstein, N., The Coordination and Regulation of Movements, Pergamon Press, Oxford,...
  • Bizzi, E., Mussa-Ivaldi, F.A. and Giszter, S., Computations underlying the execution of movement: a biological...
  • Boline, J., Ashe, J., Taira, M. and Georgopoulos, A.P., Motor cortex and isometric force: dynamic vs. static processes,...
  • Chang, H.T., Ruch, T.C. and Ward, A.A., Topographical representation of muscles in motor cortex of monkeys, J....
  • Cheney, P.D. and Fetz, E.E., Functional classes of primate corticomotoneuronal cells and their relation to active...
  • Conrad, B., Wiesendanger, M., Matsunami, K. and Brooks, V.B., Precentral unit activity related to control of arm...
  • Drew, T., Role of the motor cortex in the control of gait modification in the cat. In: M. Shimamura, S. Grillner and...
  • Evarts, E.V., Relation of pyramidal tract to force exerted during voluntary movement, J. Neurophysiol., 31 (1968)...
  • Evarts, E.V., Activity of pyramidal tract neurons during postural fixation, J. Neurophysiol., 32 (1969)...
  • Evarts, E.V., Fromm, C., Kroller, J. and Jennings, V.A., Motor cortex control of finely graded forces, J....
  • Fetz, E.E. and Finocchio, D.V., Correlations between activity of motor cortex cells and arm muscles during operantly...
  • Fetz, E.E. and Cheney, P.D., Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells,...
  • Flash, T. and Hogan, N., The coordination of arm movements: an experimentally confirmed mathematical model, J....
  • Flanders, M. and Herrmann, U., Two components of muscle activation: scaling with speed of arm movement, J....
  • Fromm, C., Changes of steady state activity in motor cortex consistent with the length–tension relation of muscle,...
  • Georgopoulos, A.P., Ashe, J., Smyrnis, N. and Taira, M., Motor cortex and the coding of force, Science, 256 (1992)...
  • Georgopoulos, A.P., Caminiti, R., Kalaska, J.F. and Massey, J.T., Spatial coding of movement: a hypothesis concerning...
  • Georgopoulos, A.P., Kalaska, J.F., Caminiti, R. and Massey, J.T., On the relations between the direction of...
  • Georgopoulos, A.P., Kettner, R.E. and Schwartz, A.B., Primate motor cortex and free arm movements to visual targets in...
  • Georgopoulos, A.P. and Massey, J.T., Static versus dynamic effects in motor cortex and area 5: comparison during...
  • Georgopoulos, A.P., Schwartz, A.B. and Kettner, R.E., Neuronal population coding of movement direction, Science, 233...
  • Ghez, C., Contribution of central programs to rapid limb movement in the cat. In: H. Asanuma and V. Wilson (Eds),...
  • Ghez, C. and Vicario, D., The control of rapid limb movement in the cat. I. Response latency, Exp. Brain Res., 33...
  • Ghez, C. and Vicario, D., The control of rapid limb movement in the cat. II. Scaling of isometric force adjustments,...
  • Gibson, A.R., Houk, J.C. and Kohlerman, N.J., Relation between red nucleus discharge and movement parameters in trained...
  • Giszter, S.F., Mussa-Ivaldi, F.A. and Bizzi, E., Convergent force fields organized in the frog's spinal cord, J....
  • Graham Brown, T. and Sherrington, C.S., On the instability of a cortical point, Proc. R. Soc. Lond. Ser. B, 85 (1912)...
  • Grobstein, P., Organization in the sensorimotor interface: a case study with increased resolution. In: J.-P. Ewert and...
  • Grobstein, P., Between the retinotectal projection and directed movement: topography of a sensorimotor interface, Brain...
  • Hepp-Reymond, M.-C. and Diener, R., Neural coding of force and of rate of force change in the precentral finger region...
  • Hepp-Reymond, M.-C., Wyss, U.R. and Anner, R., Neuronal coding of static force in the primate motor cortex, J. Physiol....
  • Hoffman, D.S. and Luschei, E.S., Responses of monkey precentral cortical cells during a controlled biting task, J....
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