From Eye to Hand: Planning Goal-directed Movements
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)
- et al.
Mechanical properties of muscles: implications for motor control
Trends in Neuroscience
(1982) - et al.
Internal representation of gaze direction with and without retinal inputs in man
Neuroscience Letters
(1995) Localization of objects in the peripheral visual field
Behavioral Brain Research
(1993)Movement without proprioception
Brain Research
(1974)- et al.
Ocular proprioception and efference copy in registering visual direction
Vision Research
(1991) - et al.
Effect of context and efference copy on visual straight ahead
Vision Research
(1989) Multiple sources of outflow in processing spatial information
Acta Psychologica
(1986)- et al.
Pointing movement in an artificial perturbing inertial field: a prospective paradigm for motor control study
Neuropsychologia
(1996) - et al.
The use of egocentric and exocentric location cues in saccadic programming
Vision Research
(1995) - et al.
Discrete vs continuous visual control of manual aiming
Human Movement Science
(1991)
Exploring the third dimension with eye movements: better than stereopsis
Vision Research
Distance- and error-related discharge of cells in premotor cortex of rhesus monkeys
Neuroscience Letters
Interaction of stereo and texture cues in the perception of three-dimensional steps
Vision Research
Human arm trajectory formation
Brain
Movement control hypothesis: a lesson from history
Behavioral and Brain Sciences
Do cortical and basal ganglionic motor areas use “motor programs” to control movement?
Behavioral and Brain Sciences
A minimum energy cost hypothesis for human arm trajectories
Biological Cybernetics
Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque
The Journal of Neuroscience
Encoding of spatial locations by posterior parietal neurons
Science
Kinematic features of unrestrained vertical arm movements
The Journal of Neuroscience
Activity in the precentral motor areas after presentation of targets for delayed reaching movements varies with the initial arm position
European Journal of Neuroscience
La vibration des muscles de la nuque modifie la position apparente d'une cible visuelle
Comptes Rendus de l'Académie des Sciences de Paris
The contribution of coordinated eye and head movements in hand pointing accuracy
Experimental Brain Research
The coordination of eye, head and arm movements during reaching at a single visual target
Experimental Brain Research
Does the nervous system use the equilibrium point control to guide single and multiple joint movements
Behavioral and Brain Sciences
Computations underlying the execution of movement: a biological perspective
Science
Posture control and trajectory formation during arm movement
The Journal of Neuroscience
Effect of load disturbances during centrally initiated movements
Journal of Neurophysiology
Mechanisms underlying achievement of final head position
Journal of Neurophysiology
Reference systems for coding spatial information in normal subjects and a deafferented patient
Experimental Brain Research
Error accumulation and error correction in sequential pointing movements
Experimental Brain Research
Motor control prior to movement onset: preparatory mechanisms for pointing at visual target
Experimental Brain Research
Goal-directed arm movements in absence of visual guidance: evidence for amplitude rather than position control
Experimental Brain Research
Contribution of retinal versus extraretinal signals towards visual localization in goal-directed movements
Experimental Brain Research
The dorsomedial frontal cortex of the macaca monkey: fixation and saccade-related activity
Experimental Brain Research
Specification of direction and extent in motor programming
Bulletin of Psychonomic Society
Error analysis, regression and coordinate systems
Behavioral and Brain Sciences
Effects of gaze on apparent visual responses of frontal cortex neurons
Experimental Brain Research
Relation between cognitive and motor-oriented systems of visual position perception
Journal of Experimental Psychology
The absence of position sense in the human eye
Journal of Physiology
Head position signals used by parietal neurons to encode locations of visual stimuli
Nature
Influence of extraocular muscle proprioception on vision
Physiology Reviews
Comparison of frontal and parietal lobe spatial deficits in man: extrapersonal and personal (egocentric) space
Perceptual and Motor Skills
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