On Sensory and Automatic Control of Movement

142 ON SENSORY AND AUTOMATIC CONTROL OF MOVEMENT,

M. Mashour Department of Psychology, University of Stockholm, Sweden

S'"?T8ry: The paper compares two hypotheses concerning control of goal-directed sk1lled and unskilled movements, namely, the outflow (centralist) hypothesis, which asserts that movements are controlled centrally by motor program, and the input (peripheralist) hypothesis, according to which control of movements occurs on the basis of sensory feedback. This paper argues in favor of the input hypothesis, regarding movements as autonomous rather than automatic processes. In support of the input hypothesis the results of an experiment on pursuit eye movement are presented and, finally, two movement control models are briefly discussed. Goal-directed movements as spatio-temporal output patterns of muscles - and as the executive bases of orientation, locomotion, communication, and manipulative behaviour of the human organism - are voluntary movements in the sense that they start and can be modified and ceased at will. Goal-directed movements comprise both unskilled and skilled movements. The, term "goal" in the present context should be understood in a somewhat technical sense, namely, as a desired state or pattern of muscular movement (or its behavioural correlate) against which the actual state (pattern of movement or its behavioural correlate) can be checked. The following cases are two examples of a goal according to this definition: a'point or an object as a desired positional state in the physical environment ('in locomotion), and a memory (stored) pattern of a word as a desired pattern against which the spoken word (the behavioural' correlate of the muscular movement pattern) can be checked. To the extent'that the actual state of movement can be compared with the desired state and, if necessary, corrected, the underlying mechanism may be regarded as functionong more or lesJ analogously to a feedback-control system - a servomechanism, This closed-loop model of movement control has been adopted by many cybernetically oriented investigators (see e.g. Smith /15; Annet /1, for review). Since sensory information initiating in the periphery (sense organs) enters the central mechanism, the abov-mentioned control model has been called alternatively the "input" or "peripheralist" hypothesis versus the "output (outflow)" or "centralist" hypothesis (Glen' cross /5). According to the latter hypothesis, skilled movements are preprogrammed (automatized) by a central control mechanism where "knowledge of the movement results from the monitoring of the efferent or output signal, rather than by any sensOry input". In its principal features, this point of view is held by Helmhotz in his' classical work Handbuch der physiologischen Optik, Lashley /9, Keele /7, and

143 others • In the controversy between the centralist and the

peripheralist~

this paper argues

in favor of the latter, that is, for the necessity of feedback (sensory) information in the control of movement (voluntary control). The outflow hypothesis The nature of evidence reported in the litterature in support of the centralist hypothesis can be characterized as follows. (a) Since the hypoyhesis is based on an assumed central control mechanism which is not amenable to direct observation (at least so far), the evidence is only indirect. (b) The most convincing evidence can be provided-by sensory bloc~ge studies provided (i) that all the relevant internal (proprioceptive) and external (visual,

au~

ditory, etc) sensory feedback channels are blocked, and (ii) that the blockage acts: for a ~ong period so that one can a'scertain the extent to' wich the hypothesized mo- ' " tor program can continue without

deteri~rating

(in the absence of sensory reinforce-

ment). For obvious reasons, sensory blockage under these conditions can probably be, realized only with infrahuman animals. Such studies, however, as indicated by • re-' cent comprehensive review (Glencross /5), have employed only partial blockage, implying that the animals could have used other sensory cues for performing (though often abnormally) the movements under study: for example, swallowing movements in mammals (Doty, Richmond, and Storey /3), movements related to bird vocalizations (Konishi and Nottebohm /8) and locust's wings (Wilson /18). In these examples, "deafferentation" was applied as a means of achieving sensory blockage. (c) Other indirect evidence comes from studies on the organization of movements in' complex skills such as piano playing and speaking. It is

a~ued

that a complex skill

consists of a series of movements which occur in a definite order and in rapid succession - "faster than visual or kine!lthetaic feedback 10C/ps". According to one estimation~

the speech apparatus involves several hundred individual muscular events

every second (Lenneberg /11) - a rate which is certainly far above the capacity-for movement control by sensory information (approximately 5 corrections every second)., This high rate of muscular events neither justifies the need for control by motor program, nor excludes the necessity of control by sensory information. The nature of sensory control will be discussed later in this

p~per.

Skilled performance (movement) does not dispense with the sensory control of behaviour; it just decreases the size and the number of errors, thereby reducing the number of corrective actions. This reduction increases the amount of spare time that, is available for the processing of sensory information. This means that, contrary to the centralist's view, there is more opportunity fbr sensory monitoring (due to reduced corrective actions) in skilled than unskilled perfo~ance (movemeut). (d) The speed of saccadic movements is considered to support the outflow hypothesia.

144 For example, saccadic movements extending 1 to 20 degrees take only 10 to 70 msec. (Yarbus /19), indicating that saccades cannot be controlled by sensory feedback loops during their running course because these loops take longer. This is a plausible argument in support of automatic motor control, yet in one essential sense sensory control is necessary: namely, that saccades being goal-directed movements, need correcti~e

action at their termination if the position of the visual axis (the actual

output) deviates from the target. This control cannot be exerted centrally by motor program, but rather by sensory feedback. In this fundamental sense, there is no difference between fast (saccadic) and slow movements. The following experiment on pursuit eye movement provides partial evidence against mptor program and in favor of the use of sensory feedback for control of movement. Three subjects were asked to follow a spot of light on a~ oscilloscope screen as accurately as possible. The track was horizontal, subtending an angle of about 2.4 degrees. The eye movements were recorded at the following target velocities: 7, 12, 20, 35, 50, 70, 120, 150, and 250 minutes of arc/sec. The recording instrument was based on the corneal ref1exion principle and photoelectric registration technique .(for details of the experiment, see Mashour /12). Fig. 1 is a sample of the recorded eye movements at 3 different velocities and can be regarded as representative of the common features- of eye movements at all velocities used in the experiment.

, I N

t

• I

M

Fig. 1. The original registrations of the eye movements of a subject during pursuit(A-D). The trace in each graph consists of horizo~tal and oblique lines representing eye pauses and eye movements respectively. Graph (a) is a control record. The recording paper was moving at 100 mm/sec. The traces are from the left eye. As can.be seen in Fig. 1 the traces are not regular smooth curves, consisting rather of a number of short oblique lines, corresponding to saccadic movements, interspersed with horizontal lines corresponding to fixation durations varying between 0.1 and 0.3 sec. The traces indicate that pursuit movement consists of a number of voluntary fixations (when the eye is practically stationary) interrupted by short periods of saccadic movements. The saccades seem to occur whenever the target (image) leaves the central fovea. The deviation of the target from the fovea in fact serves as sen-

145 sory feedback for correction of the eye's position by saccadic movementa, implying that eye movements - at least under the experimental conditiona described above are not controlled by a central motor program (i.e. automatically). This applied, moreover, to movement conditions that were quite simple and predictable, particulary the motion track (always tha same horizontal line ot constant length). (e) Other categories of evidence that have been mentioned in support of the outflow hypothesis include latency and ischemic nerve block studies (see Glencross /5, for review). The former are mainly concerned with anusally rapid amendent movements, i.e. corrective -reactions to wrong responses observed above all in some manual tracking situations. The delay for amended responses is so short - about 60 to 90 msec. - that corrections cannot employ the

senso~

feedback loop. In ischemic nerve-block tech-

nique, on the other hand, a pressure cuff is applied to a human limb in order to block kinesthetic feedback before motor functions deteriorate (see Laszlo and Bairstow /10). However, since for methodological reasons,the findings of latency and ischemic nerve block studies are not well established, they will not be commented ori further here. The input hypothesis In contrast to the outflow hypothesis there is direct evidence in support of the control of movement by sensory feedback - the input (peripheralist) hypothesis. The evidence is "direct" in the sense that performance deteriorates during sensory blockage and becomes normal again (immediately or gradually) if the blockage is removed. This has been shown by extensive studies, particulary on delayed and disrupted visual feedback (e.g. Smith /15) and auditory feedback (e.g. Fairbanks /4; Deutsch and Clarkson /2; Sussman and Smith /16; Yates /20,/21, for review). Performance deterioration as a result of delayed and disrupted feedback is, at the same time, strong indirect evidence against the centralist hypothesis, since this type of deterioration cannot be explained by the concept of motor program in that hypothesis. l

Central control and sensory data The outflow hypothesis can also be criticized on other grounds, namely, the fact that all movements, be they skilled or unskilled, are performed in the environment, where the conditions relevant to the performance usually vary in an unpredictable manner. These unpredictable variations cannot be included in the motor program - they should rather be detected by sensory feedback, that is, during the actual execution of the movement. Another related problem in this connection is the almost insurmountable difficulty that arises in connection with control by motor program , namely, transformation of physical magnitudes (measures) into valid program (subjective) measures. Without such metric transformations, the motor program cannot execute a correct

p~ttern

of move-

146 ment. And this, in fact, is the case, for man is not a measuring, instrument, he is particulary incapable of measuring (estimating) physical,magnitudes on a valid interval or ratio scale basis (Nash /4; Guilford /6; Mashour and Hosman /13; and others). Sensory feedback is, therefor. indispensible fOr the correction of deviations that arise from the inaccurate metric aspects of the movement pattern. Glencross /15 has recently proposed a two-stage model of movement control which is based on Welford's /17 three-stage central mechanism. The first stage is an executive control system that is closed-loop or feedback dependent, and the second stage "incorporates an open-loop system in the form of a mptor program, which, once initiated, will normally run its full course without any further sensory or central intervention." The model thus integrates the non-controlling motor program and the controlling executive system (based on sensory feedback) into a unified mechanism. This paper adopts a'position that is somewhat similar to Glencross' model, namely: a pattern of movement consists of a number of critical subpatterns which have been aquired and stored in the central mechanism. They function both as the executive program' and as th~ control program. As executive p~ogram, the subpatterns acivate specific groups of muscles

(moto~patterns)

in a definite serial order, and as control

program the same subpatterns (desired outputs) are compared with the executed movement patterns provided by sensory feedback (actual outputs). If the actual and the desired outputs do not match, the motor (muscular) subpattern is corrected. In this model sensory feedback is essential for at least two reasons, namely: for control of actual patterns (outputs), and for preventing perceptual and motor patterns from being forgotten (here sensory feedback functions as reinforsement or rehearsal). As can be seen, central control by motor program is entirely ruled out in this model. Both skilled and unskilled movements are considered as autonomous rather than automatic processes. \ \

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