Human Movement Science 3 (1984) 285-299

North-Holland

285

BRAIN INJURY AND MOVEMENT RECALL: PRESELECTION, ACTIVE-PASSIVE AND INTERFERENCE EFFECTS *

Roger ADAMS Cumberland College of Health Sciences, Australia

Sally ANDREWS University of New South Wales, Australia

Adams, R.D. and S.M. Andrews, 1984. Brain injury and movement recall: preselection, active-passive and interference effects. Human Movement Science 3, 285-299.

Stroke patients with unilateral lesions were compared with age-controls and students on their

ability to reproduce a terminal location established kinesthetically by a previous movement.

Conditions for the criterion movement differed over active/passive and preselected/constrained

(experiment 1) and whether the retention interval between the criterion and recall movements

involved mental rehearsal of the criterion movement or yes/no responding to a mental arithmetic

task (experiment 2). Whereas students showed more accurate recall with little effect of criterion

movement condition, patient groups showed a preselection effect, but only with active movements.

A preferred hand advantage observed for the patient controls did not occur with stroke patients,

and prevention of mental rehearsal during the retention interval disrupted recall more for the

stroke patients. These findings are interpreted in terms of hemisphere-specific coding strategies

whose relative use depends on the attentional demands of the task.

Comparisons of the short-term motor memory of unilaterally brain-in- jured patients with cerebrally uninjured controls may have implications for an understanding of the mechanisms mediating motor memory in the normal population, particularly in view of the current concern with hemispheric specialization in motor memory (Kimura 1977; Roy and Elfeki 1978; Roy and MacKenzie 1978). More practically, such com-

* This research was supported by the Australian Research Grants Commission. The authors wish to express their gratitude to the Physiotherapy staff and patients at Lidcombe

Hospital for their co-operation. Mailing address: R. Adams, Cumberland College of Health Sciences, Lidcombe, P.O. Box 170,

N.S.W. 2141. Australia.

0167-9457/84/$3.00 0 1984, Elsevier Science Publishers B.V. (North-Holland)

286 R. Adams, S. Andrew / Brain rnjury and mouement recall

parisons may provide data relevant to the rehabilitation of stroke patients. Given that the success of skill relearning techniques depends ultimately on a patient’s ability to encode appropriate movement information in short-term memory and transfer it to long-term memory, theories of motor skill acquisition and performance are relevant to physiotherapy with many neurological disorders (Carr and Shepherd 1982; Marteniuk 1979).

However, just as research on therapy for brain-injured populations has failed to comprehensively explore basic behavioural applications (Horton and Howe 1981; Miller 1980), so investigations of the motor behaviour of the brain-injured have tended to ignore the issues which have dominated theorizing about motor behaviour in normals. The present research was directed towards rectifying this omission.

One of the manipulations which has had substantial impact on theories of motor memory and behaviour is that of encouraging sub- jects to determine in advance (preselect) the terminal location of the movement they will later have to recall (Stelmach et al. 1975). This condition is typically compared with one in which the terminal location is determined (constrained) by the experimenter placing a stop. A number of experiments using a variety of paradigms have established that preselected movements are recalled more accurately than con- strained movements (eg., Kelso and Wallace 1978; Stelmach 1977), but there is still considerable controversy concerning the explanation of this phenomenon. Early focussing on motor mechanisms (Jones 1974) ap- pears untenable in view of evidence that preselection effects survive when efferent cues are eliminated via a wrist-cuff, and when afferent cues are made unreliable by variations in starting position (Kelso 1977). These data imply that movement recall relies on an internal representa- tion of spatial location rather than on memory for either the efferent or afferent activity involved in the movement.

But acceptance of this general cognitive explanation of the preselec- tion effect raises questions concerning the nature of the internal repre- sentation mediating location memory. Roy (1978) and Roy and Diewert (1978) have argued that preselection effects depend only on the provi- sion of prior information concerning the terminal location and are independent of efference. Kelso (1977) and Kelso and Wallace (1978), on the other hand, see preselection effects as reflecting an intrinsic relationship between encoding strategy and efference: prior information allows the formation of an image or movement plan which results in the

R. Adams, S. Andrew / Brain injury and mouement recall 287

‘presetting’ of appropriate sensory receptors to receive afferent signals. One way of distinguishing between these two views is in terms of the

degree to which they imply verbally-mediated as opposed to image- mediated strategies for internally representing spatial location. Roy emphasizes the fact that performance may depend on “a store compris- ing principally non-motor information” (1978: 404) and his procedure of providing prior information in constrained conditions by telling subjects that their criterion movement was to be half the distance of a previously determined standard, implies a verbally mediated strategy. In contrast, Kelso and Wallace focus on the role of “an anticipatory image” which “serves as a referent for the interpretation of incoming feedback” (1978: 105).

If this distinction between the two cognitive explanations of preselec- tion effects is accepted, then investigations of unilaterally brain-injured groups are highly relevant to an understanding of the mechanisms mediating preselection. Many studies have confirmed the fact that patients with unilateral hemisphere pathologies show hemisphere- specific deficiencies in imaginal and verbal memory coding (see Whitehouse 1981, for a review). If the preselection effect depends on the implementation of a verbally-mediated cognitive strategy, it might be expected that patients with damage to the left cerebral hemisphere would show reduced preselection effects. However, the assumption that a strategy based on an image mediates preselection would result in the opposite prediction: right-hemisphere damaged patients would be less sensitive to preselection than either left brain-injured patients or intact controls.

Experiment 1

In order to explore the relative contribution of verbal and spatial strategies to the preselection effect, unilaterally left- and right-hemi- sphere brain-injured patients were compared in terms of their memory for the terminal location of preselected and constrained movements. Both active and passive movements were required so that the contribu- tion of efferent information to motor memory could be simultaneously evaluated. Brain-injured patients were compared with both age-matched intact patients and students so that any deficits due to brain pathology could be separated from those resulting from age and/or institutionali- zation.

288 R. Adams, S. Andrew / Brarn injury and movement recall

Method

Subjects Twenty-four of the thirty-six right-handed subjects who participated

in the study were patients hospitalized in the rehabilitation wards of Lidcombe Hospital, Sydney. Twelve of these patients had suffered their first cerebra-vascular accident (stroke), which had resulted in unilateral damage, at least one month prior to testing. For six patients the injury was to the right, and for six to the left, cerebral hemisphere. The affected hemisphere was ascertained from medical records of clinical history and neurological examination which was usually supplemented by a brain scan. Further criteria for selection were the patient’s ability to comprehend instructions related to making movements with the non-affected arm (i.e., on the side ipsilateral to the lesion) and willing- ness to participate. The average ages of the left and right hemisphere-in- jured groups were 68.8 and 67.2 year, respectively. The remaining twelve patients were hospitalized in the same wards for non-brain-re- lated disorders (e.g., limb amputations) and had average ages of 67.8 and 70.1 for the left- and right-hand control groups, respectively. In addition, twelve right-handed undergraduate students (average age 20.2 years) completing their Physiotherapy degrees at Cumberland College of Health Sciences, Lidcombe, took part.

Apparatus The movement apparatus was a standard angular positioning device,

consisting of a padded arm rest attached by a single pivot to a metal frame. With the subject seated facing the apparatus and his or her forearm supported on the arm rest, movements could be performed from full elbow extension through to 90 degrees of elbow flexion. A curved degree scale on the metal base, and a pointer on the arm rest allowed measurement accuracy of within 1 degree, and a movable metal screw on the outside arc of the apparatus enabled the experimenter to limit the extent of the movement in the constrained conditions. Subjects were blindfolded during testing.

Task The task was designed to assess memory for spatial location. Each

trial consisted of two movements: a criterion movement (CM) of the arm away from the body which established the to-be-remembered

R. Adams, S. Andrew / Brain injury and movement recall 289

location; and a recall movement (RM). In order to ensure that terminal location rather than movement extent was being remembered, the starting position of the RM was varied.

Design The between-groups factors manipulated were brain status (injured-

aged/intact-aged/intact-young) and hand tested (right/left). For the brain-injured groups hand of testing was perfectly correlated with hemisphere of lesion because these patients could only be tested with their non-affected (ipsilateral) arm. Hand of testing was therefore manipulated for the control patients and students such that six subjects in each of these groups were randomly allocated to use their right (preferred) hands and six their left (non-preferred) hands.

Three factors were manipulated within-groups. First, movements were made either actively by the subject, or passively in the sense that the subject relaxed his arm while the experimenter moved the arm rest to the terminal location. Second, criterion locations were either pre- selected by the subject or externally constrained by the experimenter. The combination of these factors resulted in four CM conditions: active-preselected, active-constrained, passive-preselected and passive- constrained. The starting position for the active RM was from positions - 10, - 5, + 5 or + 10 degrees from the CM starting position. This was varied over the four CM conditions in a Latin square and thus necessitated 16 trials from each subject.

Procedure Subjects were seated in front of the apparatus so that their forearm

was comfortable on the arm rest. Following both a brief description of the rationale of the experiment and a demonstration of the use of the apparatus by the tester (Fordyce and Jones 1966) they were asked to move the lever a few times with their eyes uncovered. Practice trials were then administered to ensure comprehension of the nature of the two movements comprising a trial. In these practice trials, the RM starting position always differed from the CM starting position, but at values not employed during the experiment. Subjects were then blind- folded and a response region was established for criterion movements by passively moving subjects’ arms to locations 20 and 70 degrees from the starting position. Comprehension was again tested by requesting steadily-paced movements between the boundary locations. Subjects

were asked for variation in their CM selections, and were told that the CM and RM starting positions would be different, but not about the nature or extent of the difference.

Each trial followed the same sequence. Testing began with the active-preselected condition in which subjects were told to ‘ think’ about where they were going to move to; then three seconds later, to ‘move’ to their selected position. The terminal location of the CM was re- corded and the subject’s arm was passively returned to the pre-de- termined RM starting position. Following a 10 second retention inter- val, subjects were told to go back to the position where they had stopped before and the terminal location reproduced was recorded in degrees. The next condition, active-constrained, was identical to the active-preselected condition, except that subjects were told that the experimenter would decide on the CM terminal location and that they should simply move the arm rest until stopped by an external con- straint. The terminal location used in these conditions was yoked to the preselected conditions such that the constraint was placed at the same positions as the subject had self-terminated in the previous preselected trials. The RM for the constrained conditions was identical to that for preselected movements.

Rather than subjects moving themselves in the passive CM condi- tions, they relaxed their arms while the experimenter moved the arm rest. In the passive-preselected condition, subjects selected the terminal location by giving the experimenter a ‘stop’ command whilst the support was being moved. The CM set for the passive-constrained condition was also yoked to the prior preselected set. Treatment condi- tions were always presented in the above order to allow for yoking and to facilitate explanation to subjects, as in this way additional informa- tion concerning the stop, then passive movements, came after experi- ence with active preselected movements.

Subjects were given short breaks between conditions and were re- minded before each trial of the nature of the specific CM condition by the instructions ‘move to where you thought’, ‘move until stopped’, ‘tell me when to stop’, and ‘I’ll move you to the stop’.

Results and discussion

Two measures were calculated from the subjects’ responses, constant error (CE), the mean algebraic error which represents bias toward

R. Adams, S. Andrews / Brarn injwy and mouement recall 291

under- or overshooting terminal location, and absolute error (AE), which represents overall accuracy. Variable error (VE) scores could not be calculated as there were no repeated measures at the different recall starting positions.

Constant error Since the influence of recall start position on location reproduction

error is indicative of the integration of distance and location informa- tion in the memory for the criterion movement (Walsh and Russell 1979, 1980), CE scores were collapsed over other conditions (table 1) to enable testing of planned contrasts across the four recall start positions. Of the linear, quadratic and cubic trend components, only a significant linear trend (F(1,30) = 29.47, p -c 0.01) emerged, indicating that sub- jects undershot for negative RM starts and overshot for positive RM starts, in the same pattern as that observed in previous studies. Main effects of groups and interactions with between-groups planned con- trasts were also tested. No significant results were found between groups or from differences in linear and quadratic trend between groups, indicating that the effects of memorial intergration of distance and location cues were similar for both brain-injured and normal subjects.

There was, however, a significant difference in cubic trend between the two patient groups (F(1,30) = 5.31, p -c 0.05). Brain-injured patients were less accurate at - 10 and + 10 than at - 5 and + 5 degrees recall starts, whereas their age-matched controls were more accurate at the more extreme starting positions. It may be that control patients were detecting, and subsequently correcting for, the more deviant recall starts while the brain-injured were not.

Table 1 Average constant error for each of the six groups in the study at each of the four possible starting positions for the recall movement.

Recall start Brain-injured Patient control Students

relative to Left hand Right hand Left hand Right hand Left hand criterion start

Right hand

-100 0.42 - 2.00 0.13 - 1.31 - 1.54 - 3.08 -5O 0.54 2.25 0.41 - 1.70 - 0.71 - 1.71 +5O 1.50 2.13 1.38 3.50 0.58 - 1.13

+lo” 4.50 5.33 2.92 1.50 0.71 1.75

292 R. Adams, S. Andrews / Bram injury and movement recall

Absolute error The absolute error data (fig. 1) were analyzed by planned contrasts

which evaluated the between-groups factors of brain status and hand of testing, the within-group factors of active/passive and preselected/con- strained, and the interactions between these factors. Students repro- duced movements with significantly less error than the combined patient groups (F(1,30) = 5.22, p -c 0.05). There was no significant difference between the overall accuracy of stroke patients (5.8 degrees) and aged controls (5.3 degrees). Hand of testing was significantly involved only in an interaction (F(1,30) = 4.58, p < 0.05) such that the preferred (right) hand advantage observable for patient controls was absent in the brain-injured groups where patients using their previously non-preferred (left) hands were as accurate as those using their right hands.

Analysis of the repeated measures data revealed a significant interac- tion between the active/passive and preselected/constrained conditions whereby preselected criterion movements were more accurately repro- duced than constrained ones in active but not passive conditions

BRAIN-INJURED PATIENT CONTROL STUDENTS

preselected constrained preselected constrained preselected constrained

Fig. 1. Average absolute error in movement reproduction for each of the six groups over the four criterion movement conditions. Within each subject classification points for subjects using their

left hands are represented by black symbols, and points for subjects using their right hands by open symbols. Error scores from active movements are represented by circles, and from passive

movements by squares.

R. Adams, S. Andrews / Brain injury and movement recall 293

(F(1,30) = 4.58, p -c 0.05). The active/passive main effect approached significance (F&30) = 4.04, p -c O.lO), but neither the preselected/con- strained main effect nor any of the interactions between the repeated measures factors and between-groups factors did so.

Overall these data support those of Kelso (1977) rather than Roy (1978). Firstly, the preselection effect obtained only for active move- ments. Such an interaction implies that efferent cues are necessary for prior information to benefit recall. Secondly, in terms of the predictions outlined previously, these results imply that movement location recall relies on spatial-image code. Patients with damage to their right hemi- sphere (using their right hand) were relatively worse than control patients using their right hand, than were left brain-injured patients as compared with controls using their left hand. The fact that right-handed students showed a marginal left-hand advantage is also in accord with the notion of the right hemisphere mediating spatial representation, and consistent with other findings of right-hemisphere superiority in spatial location tasks (Roy and Mackenzie 1978; Dalby 1980).

The greater accuracy of the patient control group using their right hand supports Kocel’s (1980) conclusion that “there appears to be increasing reliance with age on left-hemisphere strategies . . . either in response to, or provoking right-hemisphere decline” (1980: 229). Fur- ther, the return to a marginally superior left hand performance in the brain-injured groups suggests that the right hemisphere does not de- teriorate with age, but that it is simply less used when the intact left hemisphere ‘provokes’ its disuse.

Experiment 2

Besides these indications of some degree of hemispheric specialization in location memory, the results of experiment 1 also contain suggestions of attentional effects on movement recall, where attention is seen as limited central processing capacity. Both the brain-injured groups, and those control patients performing with their left hand, exhibited their worst performance when criterion movements were passive and pre- selected. In this condition, subjects had to terminate their recall move- ment with a verbal command. It seems likely that the combination of a verbal response and reduced efferent information caused this condition to be the most attention-demanding of the four investigated. In this

294 R. Adams, S. Andrews / Brarn injury and mouemen~ recall

context, the fact that students showed no effect of either the active/passive or preselected/constrained manipulations would be in- terpreted as demonstrating that all conditions were well within their attentional capacity.

The aim of the second experiment was to more directly explore the role of attention in location recall by investigating the effect of pre- venting or encouraging rehearsal of the to-be-remembered location.

Method

Subjects A further sixteen right-handed stroke patients with unilateral damage,

eight to the right and eight to the left hemisphere with average ages of 63.2 and 64.8 years respectively were selected from the Lidcombe Hospital rehabilitation wards. As an age-control group, two groups of eight right-handed subjects, from the Strathfield Lawn Bowling Club, with a mean age of 59.7 and 61.2 years, took part. None of the bowlers had suffered any brain injury, and all were in the first (highest) division.

Apparatus and task The between-groups factors manipulated were brain status

(injured/control), retention interval activity (mental rehearsal of the CM/mental arithmetic) and hand used (left/right). The starting posi- tion of the RM was - 10, - 5, + 5, and + 10 degrees from the starting position of the CM, and varied over sixteen trials (four at each RM start) in a Latin square.

Procedure Introduction of the subjects to the task was as described in the

previous experiment, with the difference that only active-preselected CMs were employed. A brief rest was given after each block of four trials, which covered all four RM starting positions. The retention interval between the CM and RM was 30 seconds, and was filled either by an interfering task or mental rehearsal of the CM. To interfere with encoding, yes/no responses were required to single-digit addition and subtraction problems, e.g., ‘Does four plus two equal seven?’ or ‘Does eight minus five equal three?. This task was selected after pre-testing with other patients showed it to be at a suitable level of complexity for

R. Adams, S. Andrew / Brain injury and movemenf recall 295

the brain-injured to make about 75% correct responses. In the mental-rehearsal conditions, subjects were encouraged on each

trial to imagine their arms returning to the previous CM terminal location.

Results and discussion

CE and AE scores were again calculated from subjects’ responses. Performance on the mental arithmetic task was 71% and 74% for the left and right brain-injured groups respectively, and this difference was not significant. No errors were made by the age-control subjects on this task.

Constant error Planned contrasts testing for trend over the four RM starting posi-

tions were applied to the data when it was collapsed across the four trials at each RM start (table 2). Both the linear (F(1,24) = 44.31, p c 0.01) and cubic (F(1,24) = 11.67, p -c 0.01) components were sig- nificant, indicating that negative RM starts resulted in undershooting and positive RM starts in overshooting, but such that the more deviant starting position (- 10 and + 10 degrees) exerted comparatively less influence than the less deviant positions (- 5 and + 5 degrees). Both trend components were also involved in significant interactions with the Brain Injury X Hand Used groups contrast (F(1,24) = 5.64, F(1,24) = 6.34, both p -c 0.05). These contrasts show that the difference in trend for the right and left brain-injured groups was different from that of their right and left controls. Whereas the right brain-injured patients

Table 2 Average constant error for each of the eight groups in the study at each of the four possible starting positions for the recall movement, LT. and M.R. are the Interfering Task and Mental

Rehearsal groups respectively.

Recall start relative to criterion start

-lo0 -5O +5O

+lo”

Brain-injured Control

Left hand Right hand Left hand Right hand

LT. M.R. ‘1.T. M.R. LT. M.R. I.T. M.R.

0.75 -0.13 - - - 3.75 -5.13 -5.00 - 3.38 3.13 2.63 3.13 -0.13 - 4.50 -2.19 - 3.31 - 1.38 - 1.88 - 0.81 3.81 -0.38 3.75 0.69 3.69 3.75 0.94 2.00 5.00 1.25 5.89 1.13 2.13 5.06 2.56 2.25

296 R. Adams, S. Andrews / Bram injury and mouemen~ recall

showed a function of CE across RM starting position which was similar to the function for the control groups, left brain-injured patients had a significantly flatter function with the greatest effect on CE being contributed by the most deviant RM starts.

Absolute error In a planned contrast analysis (fig. 2) brain-injured subjects showed

on average 6.7 degrees error in recall of active preselected movements which was significantly worse than the 4.0 degree average of their age controls (F(1,24) = 14.22; p < 0.01). When mental rehearsal of the criterion movement rather than mental arithmetic filled the 30 second retention interval, overall recall error was significantly reduced ( F( 1,24) = 9.24; p < 0.01) and this difference between mental rehearsal when encouraged or prevented was significantly greater for the brain-injured

BRAIN-INJURED CONTROL

LEFT

interfering task

mental rehearsal

10.

9-

8 -

7-

6-

5-

4-

J-

2-

1 -

\ LEFl

0-0 RIGHT

. * nterfering mental

task rehearsal

Fig. 2. Average absolute error in reproduction of active-preselected criterion movements for each

of the eight subject groups. Squares represent groups using their left hands, and circles groups

using their right hands.

R. Adams, S. Andrew / Brain injury and movement recall 291

group than for their age-controls (F(1,24) = 4.36; p < 0.05). Though the hand used in movement recall by these right-handed subjects had no overall effect on accuracy, there was an interaction between brain-in- jury and hand of testing, such that the left hand-right hand recall error difference was significantly greater for the brain-injured groups than for their age controls (F(1,24) = 5.13; p < 0.05).

These data contrast with those of experiment 1 in the sense that left-hemisphere injured patients perform less accurately than right- hemisphere patients when each are compared with the appropriate control group, although this is only true when mental rehearsal is prevented. When taken in conjunction with the results of the previous experiment these findings suggest that though location recall can de- pend primarily on a spatial-image code, the prevention of mental rehearsal forces reliance on verbal codes and so causes difficulties for patients whose left-hemisphere functioning is impaired. The fact that left- and right-hemisphere brain-injured patients performed equiva- lently when mental rehearsal was encouraged implies that it is not simply the longer retention interval that is responsible for the differen- tial effects of side of injury in the two experiments, but rather that the spatial code assumed to underlie the performance of the left-hemi- sphere damaged group is not maintainable under conditions of atten- tion demand.

General discussion

One noteworthy aspect of the present results as a whole is that, under favourable conditions brain-injured and aged patients perform only minimally less accurately than even students. This fact confirms and extends the findings of Jordan (1978) who argued that the apparent stability of kinesthetic memory with age could have implications for techniques of retraining the elderly.

In terms of theoretical explanations of the preselection effect, these findings imply that both hemisphere-specific cognitive strategies and attentional mechanisms are involved in the mediation of preselection effects. When the retention interval is brief and unfilled (experiment l), a spatial code seems sufficient, and perhaps even most efficient, for accurate location recall. This conclusion follows from the finding that left-hemisphere damaged patients were relatively more accurate than

298 R. Adams, S. Andrews / Brain injury and mouement recall

those with damage to the right hemisphere and that students were marginally more accurate with their left than their right hand. However, when attentional demands are increased by interfering with rehearsal, spatial codes do not seem sufficient. Thus, control subjects perform less accurately with their non-practised left hand than do control subjects with their right hand, and the performance of left brain-injured patients deteriorates more than that of right-hemisphere damaged patients. Similar effects of attentional demands have been observed within young intact subjects by Runnings and Diewert (1982) who found that when memory load was increased, successful performance seemed to require both temporal (left-hemisphere) and spatial (right-hemisphere) informa- tion whilst in non-attention-demanding conditions a single information source was sufficient.

In this sense, it appears that the validity of the purely cognitive (Roy 1978) versus the cognitive-efferent (Kelso 1977) explanations of pre- selection may depend on the attention demands of the particular task employed.

More generally, the data from both experiments support Shewan’s (1976) conclusion that brain-injured patients differ quantitatively rather than qualitatively from their normal counterparts. When movement conditions are optimized, and time for encoding allowed, then for the simple angular movements studied here the performance of the brain- injured is similar to that demonstrated by those without such injury.

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