From Eye to Hand: Planning Goal-directed Movements

https://doi.org/10.1016/S0149-7634(98)00004-9Get rights and content

Abstract

DESMURGET, M., D. PÉLISSON, Y. ROSSETTI AND C. PRABLANC. From eye to hand: planning goal-directed movements. NEUROSCI BIOBEHAV REV 22(6) 761–788.—The nature of the neural mechanisms involved in movement planning still remains widely unknown. We review in the present paper the state of our knowledge of the mechanisms whereby a visual input is transformed into a motor command. For the sake of generality, we consider the main problems that the nervous system has to solve to generate a movement, that is: target localization, definition of the initial state of the motor apparatus, and hand trajectory formation. For each of these problems three questions are addressed. First, what are the main results presented in the literature? Second, are these results compatible with each other? Third, which factors may account for the existence of incompatibilities between experimental observations or between theoritical models? This approach allows the explanation of some of the contradictions existing within the movement-generation literature. It also suggests that the search for general theories may be in vain, the central nervous system being able to use different strategies both in encoding the target location with respect to the body and in planning hand displacement. In our view, this conclusion may advance the field by both opening new lines of research and bringing some sterile controversies to an end.

Introduction

Decades after the pioneering works of Woodworth [273]and Bernstein [12], the neural mechanisms involved in reaching movement generation are still, to a large extent, unknown. The present paper tries to take stock of this lack of knowledge. Our goal is to describe the state of our knowledge of the mechanisms whereby a visual input is transformed into a motor command. To this end, we consider the different problems that the nervous system has to solve to generate a movement; that is, target localization, definition of the initial state of the motor apparatus, and hand trajectory formation. For all these questions, we address three issues:

  • 1.

    what are the main results presented in the literature;

  • 2.

    are these results compatible with each other; and

  • 3.

    which factors may account for the existence of possible incompatibilities between experimental observations or between theoretical models.

In our view, this triple level of investigation is essential in understanding how goal-directed movements are planned and in going beyond the limitations imposed by the classical approach of developing independent motor theories, in parallel. We believe that the original orientation given to the present review may be heuristic and helpful to improve our knowledge of the processes involved in the elaboration of motor commands. Before developing this idea in more detail we briefly introduce the main topics to be addressed.

First, this review pinpoints the key role of gaze information and retinal signals in building a sharp representation of the target location with respect to the body (Determination of the target location section). Three main topics are considered. The first one concerns the mechanisms whereby the position of a visual target is encoded in egocentric coordinates. The second one is related to the nature (afferent versus efferent) of the eye position signal used in egocentric coding. The third one investigates the possibility that target position encoding is improved by allocentric cues provided by structured visual scenes.

The second part of this review deals with the initial stage of movement planning. We investigate whether the ability to perform accurate reaching requires, in addition to a precise definition of target location, a knowledge of the initial configuration of the limb (Determination of the initial configuration of the arm section). This question is, in particular, crucial to evaluate the validity of the different models of trajectory formation.

The last part of the present review concerns the puzzling problem of trajectory formation (Trajectory formation section). For the sake of clarity, the main models proposed in the literature with respect to this topic, are grouped into three classes:

  • 1.

    the positional models derived from the equilibrium-point hypothesis;

  • 2.

    the vectorial models, which assume that the movement is programmed as a mismatch between an initial and a final state (the issue of whether this mismatch is defined in spatial or angular terms is addressed); and

  • 3.

    the optimal control models, which presuppose that movement programming is constrained by energy minimization principles.

In the Trajectory formation section, we emphasize that most of the theories presented in the literature to account for the spatio-temporal characteristics of goal-directed movements are supported by sound experimental facts. This leads us to propose the hypothesis that the nervous system is able to use different planning strategies depending upon context. From this point, it is suggested that the search for a global model of movement control, which appears as a watermark in several recent articles 179, 16, 85, 76, 201, 220, may be in vain. Arguments favoring this view are presented.

Section snippets

Initial stages of movement planning

The present section focuses on the initial programming stage of visually triggered movements. Both the nature of the information required to perform accurate reaching, and the way by which such information is acquired, are presented. We first describe the processes that encode visual target location and subsequently review arguments supporting the necessity of encoding the limb initial configuration to generate accurate responses. It is shown how these data have influenced theories of movement

Trajectory formation

Although widely addressed during the past decades, the problem of knowing how goal-directed movements are planned by the CNS still remains debatable. The main objective of the present section is to take stock of this issue. To this end, we review the main theories presented in the literature to account for the characteristics of goal-directed movements. For the sake of clarity, these theories are examined in three successive sections addressing the equilibrium-point hypothesis and its related

Concluding remarks

The purpose of this paper has been to describe the mechanisms whereby a visual input is transformed into a motor command. To address this question, we considered successively three main problems. First, how is the initially retinocentric representation of the target converted into a body-centered representation? Second, does the knowledge of the initial state of the motor apparatus constitute a prerequisite for movement planning? Third, what is the validity and the degree of generality of the

Acknowledgements

We are grateful to J. F. Soechting and C. Ghez for allowing us to reproduce figures from their original studies and to the anonymous reviewer who helped us improve this paper. We also sincerely thank Scott Grafton and Laura Payne for editing and commenting on this manuscript.

References (275)

  • J.T. Enright

    Exploring the third dimension with eye movements: better than stereopsis

    Vision Research

    (1991)
  • D. Flament et al.

    Distance- and error-related discharge of cells in premotor cortex of rhesus monkeys

    Neuroscience Letters

    (1993)
  • J.P. Frisby et al.

    Interaction of stereo and texture cues in the perception of three-dimensional steps

    Vision Research

    (1995)
  • W. Abend et al.

    Human arm trajectory formation

    Brain

    (1982)
  • G.C. Agarwal

    Movement control hypothesis: a lesson from history

    Behavioral and Brain Sciences

    (1992)
  • G. Alexander et al.

    Do cortical and basal ganglionic motor areas use “motor programs” to control movement?

    Behavioral and Brain Sciences

    (1992)
  • R.M. Alexander

    A minimum energy cost hypothesis for human arm trajectories

    Biological Cybernetics

    (1997)
  • R.A. Andersen et al.

    Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque

    The Journal of Neuroscience

    (1990)
  • Andersen, R. A., The role of the inferior parietal lobule in spatial perception and visual–motor integration. In The...
  • R.A. Andersen et al.

    Encoding of spatial locations by posterior parietal neurons

    Science

    (1985)
  • Asada, H. and Slotine, J. J. E., Robot Analysis and Control. John Wiley and Sons, New York, 1986, pp....
  • C.G. Atkeson et al.

    Kinematic features of unrestrained vertical arm movements

    The Journal of Neuroscience

    (1985)
  • E. Bauswein et al.

    Activity in the precentral motor areas after presentation of targets for delayed reaching movements varies with the initial arm position

    European Journal of Neuroscience

    (1992)
  • Becker, W., Metrics. In The Neurobiology of Saccadic Eye Movements, ed. R. H. Wurtz and M. E. Golberg. Elsevier,...
  • Bernstein, N., The Coordination and Regulation of Movements. Pergamon, Oxford,...
  • B. Biguer et al.

    La vibration des muscles de la nuque modifie la position apparente d'une cible visuelle

    Comptes Rendus de l'Académie des Sciences de Paris

    (1986)
  • B. Biguer et al.

    The contribution of coordinated eye and head movements in hand pointing accuracy

    Experimental Brain Research

    (1984)
  • B. Biguer et al.

    The coordination of eye, head and arm movements during reaching at a single visual target

    Experimental Brain Research

    (1982)
  • E. Bizzi et al.

    Does the nervous system use the equilibrium point control to guide single and multiple joint movements

    Behavioral and Brain Sciences

    (1992)
  • E. Bizzi et al.

    Computations underlying the execution of movement: a biological perspective

    Science

    (1991)
  • Bizzi, E. and Mussa-Ivaldi, F.A., Geometrical and mechanical issues in movement planning and control. In Foundations of...
  • E. Bizzi et al.

    Posture control and trajectory formation during arm movement

    The Journal of Neuroscience

    (1984)
  • E. Bizzi et al.

    Effect of load disturbances during centrally initiated movements

    Journal of Neurophysiology

    (1978)
  • E. Bizzi et al.

    Mechanisms underlying achievement of final head position

    Journal of Neurophysiology

    (1976)
  • J. Blouin et al.

    Reference systems for coding spatial information in normal subjects and a deafferented patient

    Experimental Brain Research

    (1993)
  • O. Bock et al.

    Error accumulation and error correction in sequential pointing movements

    Experimental Brain Research

    (1993)
  • O. Bock et al.

    Motor control prior to movement onset: preparatory mechanisms for pointing at visual target

    Experimental Brain Research

    (1992)
  • O. Bock et al.

    Goal-directed arm movements in absence of visual guidance: evidence for amplitude rather than position control

    Experimental Brain Research

    (1986)
  • O. Bock

    Contribution of retinal versus extraretinal signals towards visual localization in goal-directed movements

    Experimental Brain Research

    (1986)
  • L. Bon et al.

    The dorsomedial frontal cortex of the macaca monkey: fixation and saccade-related activity

    Experimental Brain Research

    (1992)
  • M. Bonnet et al.

    Specification of direction and extent in motor programming

    Bulletin of Psychonomic Society

    (1982)
  • F.L. Bookstein

    Error analysis, regression and coordinate systems

    Behavioral and Brain Sciences

    (1992)
  • D. Boussaoud et al.

    Effects of gaze on apparent visual responses of frontal cortex neurons

    Experimental Brain Research

    (1993)
  • Brady, J. M., Hollerbach, J. M., Johnson, T. L., Lozano-Perez, T., and Manson, M. T., Robot Motion: Planning and...
  • Bridgeman, B., Complementary cognitive and motor image processing. In Presbyopia Research: From Molecular Biology to...
  • B. Bridgeman et al.

    Relation between cognitive and motor-oriented systems of visual position perception

    Journal of Experimental Psychology

    (1979)
  • G.S. Brindley et al.

    The absence of position sense in the human eye

    Journal of Physiology

    (1960)
  • P.R. Brotchie et al.

    Head position signals used by parietal neurons to encode locations of visual stimuli

    Nature

    (1995)
  • P. Buisseret

    Influence of extraocular muscle proprioception on vision

    Physiology Reviews

    (1995)
  • N. Butters et al.

    Comparison of frontal and parietal lobe spatial deficits in man: extrapersonal and personal (egocentric) space

    Perceptual and Motor Skills

    (1972)
  • Cited by (252)

    • End in view: Joint end-state comfort depends on gaze and extraversion

      2021, Human Movement Science
      Citation Excerpt :

      When humans have to grasp and transport an object, they need a coordinated interplay between body and eye movements to perform the task successfully. In the past, most studies investigated either movement kinematics (e.g., Desmurget, Pélisson, Rossetti, & Prablanc, 1998; Jeannerod, 1986) or gaze behavior (e.g., Hayhoe, Shrivastava, Mruczek, & Pelz, 2003; Land, Mennie, & Rusted, 1999) separately. Up to now, only a few studies investigated both variables synchronously during object manipulation (e.g., Kurz, Hegele, Reiser, & Munzert, 2017; Latash & Jaric, 2002; Lavoie et al., 2018), but no study investigated them synchronously in a joint action task.

    • Fundamentals of human movement, its control and energetics

      2020, Comparative Kinesiology of the Human Body: Normal and Pathological Conditions
    View all citing articles on Scopus
    View full text