E L S E V I E R Schizophrenia Research 17 (1995) 267-278

SCHIZOPHRENIA RESEARCH

Manual performance in leukotomized and unleukotomized individuals with schizophrenia

Heather Carnahan a,,, Digby Elliott b and Varadaraj R. Velamoor c

"Department of Kinesiology, University of Waterloo. Waterloo, Ont. N2L 3G1. Canada b Department of Kinesiology, McMaster University, Hamilton, Ont., Canada c Department of Psychiatry, University of Western Ontario and

Victoria Hospital, London, Ont., Canada

Received 2 June 1994; revision received 16 January 1995; accepted 27 January 1995

Abstract

Seven leukotomized adults with schizophrenia (LS), eight unleukotomized adults with schizophrenia (ULS), and eight healthy control (C) individuals were required to reach toward and grasp a small object that was either stationary or moving. Reflective markers were placed on the subject's index finger, thumb and wrist, and movements were videotaped. As expected the LS and ULS groups moved slower than the C group when the target was stationary. However, when the target was moving, all three groups moved faster, with the LS and C groups having the same movement times, and the ULS group having the fastest movement time. When the timing of the reaching trajectory was assessed, the LS group spent less time decelerating and closing their hands around the object, indicating their movements were controlled with less precision. When grasp formation was analyzed, for the stationary condition, the maximum apertures of the LS and ULS groups were not different, and both were larger than those of the C group. For the moving target condition, aperture increased for all groups but was smallest for the C group, intermediate for the LS group and largest for the S group. There was actually less within subject variability in peak aperture and maximum aperture closing speed for the LS and ULS groups in comparison to the C group, perhaps indicating a limited repertoire of potential motor responses for the patient groups. These results suggest that individuals with schizophrenia are able to use redundant information as well as controls, and that leukotomized individuals with schizophrenia have greater motor control deficits than unleukotomized schizophrenics.

Keywords: Target movement; Prehension; Leukotomy; (Schizophrenia)

1. Introduction

Historically, the study of movement in both physiology and psychology has provided insight into how the human functions, ranging from how

* Corresponding author. E-mail: carnahan@healthy.uwaterloo.ca

0920-9964/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved SSDI 0920-9964 ( 95 ) 00009-7

we use information, to how we acquire skills (King, 1976). However, despite this, the study of movement has only recently been used to help us understand more about psychiatric illnesses such as schizophrenia. Manschreck (1983; 1986) has categorized many of the motor abnormalities that have been noticed since the early definitions of the disorder, into descriptive categories associated with either increased motor activity, decreased motor

268 H. Carnahan et al. /Schizophrenia Research 17 (1995) 267-278

activity, postural disturbances or neuroleptic related disorders. One problem with studying motor disorders using the clinical descriptions used by Manschreck is that it is difficult to accurately and objectively quantify the seriousness or improvement of a motor disorder. Another approach is to use laboratory measures such as reaction time (RT) or movement time (MT) to quantify motor performance, where RT is used to measure the movement planning process, and MT reflects movement execution (see King, 1976, for a review). The general finding from this approach has been that individuals with schizophrenia exhibit a generalized slowing, and the degree of impairment is related to the degree of psychosis.

While the examination of the temporal aspects of movement has provided some understanding of the nature of the motor deficits observed in individ- uals with schizophrenia, there are other more sophisticated ways in which movement can be examined (Carnahan, 1993). Kinematic analyses provide information about how a movement is generated in terms of the displacement, velocity or acceleration (Enoka, 1988; Winter, 1990). The kinematic approach has been recently used quite successfully to quantify movement disorders in various populations with neurological damage (see Carnahan, 1993). This usually entails using either videotape or an optoelectric system devised to record a movement as it is generated. The video or digital record of the movement is evaluated frame by frame to get an accurate quantitative description of, for example, the limb trajectory when making a reaching movement. This displace- ment record can, among other things, be differentiated to calculate the speed at which the limbs move as a function of time. While an out- come measure (such as successfully picking up an object) between groups may be equal, the manner in which these seemingly similar outcomes are achieved may be very different. For example, a patient who is recovering from stroke may be able to reach out and pick up a glass. Based on out- come, their performance would be the same as a healthy control's. However, if one examines how this simple skill is accomplished, the kinematics of the patient's movement would be quite different from that of the control subject, suggesting very

different motor control strategies are being used to generate the movement. In this present study, the kinematic approach has been used to examine how individuals with schizophrenia generate reach- ing and grasping movements, to gain some insight into the degree and nature of their motor impairment.

One motivation for this study was based in part on work by Manschreck and colleagues (1981, 1985) who suggested that adults with schizophre- nia are unable to use redundant information as well as control individuals. Based on information theory "any event can be regarded as redundant to the extent that its occurrence and characteristics are predictable from observation of immedi- ately preceding events" (Manschreck et al., 1985, p. 991). The conclusion that persons with schizo- phrenia cannot make as effective use of redundant information as healthy individuals was based on a study in which schizophrenics were required to tap out a rhythm with their finger which was provided to them by acoustic clicks of various rates. It was found that they had impaired tapping ability despite the auditory guidance; that is, they were unable to efficiently use the redundant information which was provided to them. This finding is consis- tent with research examining language production and listening (Lewinsohn and Elwood, 1961; Manschreck et al., 1979; Maher et al., 1980). Another example of a highly redundant situation is one where an object is moving at a predictable velocity and path. If an individual is able to make use of redundant information they should be able to predict or anticipate where an object is going to be in both space and time, based on where it has previously been. Manschreck et al. (1985) predict that individuals with schizophrenia will not be able to make as effective use of redundancy as normal healthy control subjects in a predictable situation where they are required to capture an object moving on a fixed course and velocity. Thus to test this prediction, in the present study, individ- uals with schizophrenia were required to reach and grasp a small object as it rolled at a constant acceleration and predictable path, down a ramp. The kinematics of the reaching movement were examined to provide insight into motor planning

H. Carnahan et al./Schizophrenia Research 17 (1995) 267-278 269

and control processes to evaluate how effectively the redundant information was used.

A second purpose of this study was to examine the role of the frontal lobes in the planning and control of reaching movements. It is suggested that the frontal lobes play an important role in the control of finely skilled hand movements (Kolb and Wishaw, 1990). This is of particular interest because it has been suggested that schizophrenia is associated with a dysfunctional prefrontal cortex (Andreasen et al., 1986; Goldberg et a1.,1989; Liddle, 1990; Weinberger et al., 1986). The frontal leukotomy was introduced as a potential treatment for schizophrenia based on the rationale that by creating lesions in this area, abnormal brain activ- ity originating from this region would be prevented from spreading to other parts of the brain and potentially contributing to the severity of the symp- toms (Greenblatt and Solomon, 1953). When one observes voluntary movement deficits in schizo- phrenic individuals, it is not clear whether they are caused by something that is related to schizo- phrenia in general, or caused specifically by a damaged frontal lobe (Carnahan et al., 1994). Thus, m the present study, the motor performance of a group of leukotomized schizophrenics, unleu- kotomized schizophrenics and control subjects were compared when performing the task of reach- ing toward moving targets, to see if surgically created frontal lesions result in any differences in how movements are generated.

2. Methods

2.1. Subjects

Seven bilateral frontally leukotomized males with schizophrenia (mean age of 66.4 years, range 61 to 73 years) participated in this study. Six were right handed one was left handed. Eight right handed unleukotomized males with schizophrenia (mean age 70.4 years, range 58 to 79) served as psychiatric control patients. Eight males (mean age of 73.3 years, range 71 to 76 years) recruited from a local war veterans legion served as the age-matched control subjects. Seven were right- handed, one was left-handed.

The patients were chronic schizophrenics with residual features. They had histories of acute epi- sodes but currently showed persisting signs of the illness in the absence of prominent psychotic symp- toms within three months of testing. Emotional blunting, social withdrawal, eccentric behavior, illogical thinking and mild loosening of associa- tions were common. There was an absence of prominent delusions, hallucinations, incoherence or grossly disorganized behavior. All patients scored within normal ranges on standardized I.Q. testing. Drug status is listed in Table 1.

All schizophrenic patients were classified under the DSM-III diagnostic criteria (American Psychiatric Association, 1980). Diagnosis of schizophrenia was determined by chart review by

Table 1 Drug status

Unleukotomized schizophrenics Leukotomized schizophrenics

Subject code Medications Subject code Medications

S1 $2 $3

$4 $5 $6 $7 $8

Stelazine 5 mg tid L1 Mellaril 150 mg @ hs L2 CPZ 100 mg qid; Lithium Carbonate 300 mg L3 bid & hs Pimozide 4 mg @ 0800 L4 Doxepin 25 mg@ hs; Nozinan 5 mg @ hs L5 Clonazepam 0.25 mg qid L6 Mellaril 50 mg tid; Mellaril 100 nag @ hs L7 Stelazine 2 mg @ 12 & 17;Doxepin 10 mg @ hs

Haldol 4 mg @ hs Dilantin 100 mg qid; Mysoline 250 mg bid Nil

Mellaril 150 mg @ hs; Mellaril 50 mg @ 0800 Haldol 2 mg po qid; Cogentin 1 mg@ hs Largactil 75 mg bid & hs Clonazepam 1.5 mg@ hs

270 H. Carnahan et al./Schizophrenia Research 17 (1995) 267-278

two psychiatrists. Several physicians in the past had concurred with the diagnosis of schizophrenia in these individuals. The psychiatric patients were institutionalized at the Westminster Campus of Victoria Hospital, which was a chronic care facility for war veterans sponsored by the Department of Veterans Affairs (DVA) that has since testing been closed.

The individuals who had been operated on had received sectioning of the connections of the fron- tal cortex with other parts of the brain, particularly with the thalamus (corticothalamic tract). This procedure aimed to reduce intolerable restlessness, anxiety and morbid preoccupation. In addition it attempted to achieve (socially and subjectively) a shallower, more agreeable mood state. It is not clear why the age matched schizophrenic controls did not receive surgery. Possible reasons were: they may have responded to pharmacotherapy; they were not deemed as severe or intractable in terms of intensity of delusions, thought disorder, halluci- nations, or obsessive compulsive behavior; or there may have been problems getting consent for the surgery.

2.2. Apparatus

Individuals were seated in a chair with both hands resting on the table in front of them. As seen in Fig. 1, directly in front of them was a ramp

Position

Fig. 1. A schematic of the experimental set-up.

65 cm long with small grooves embedded on the top surface. A small cube (6.5 cm by 2.9 cm by 2.5 cm) attached to four, 1 cm wheels was rolled down the ramp and the purpose of the grooves was to ensure that the cube travelled in a straight line. Thirty cm down the ramp there was an 8 cm target zone. Twenty-eight cm below the target zone there was a start position for the subject's hand. When the cube rolled into the target region, it was grasped and lifted off the ramp. The speed of the travelling cube was modified by tilting the ramp. The ramp was raised 11 cm for the slow condition and 14.5cm for the fast condition, which translated to the ramp being at 10 degree and 13 degree angles respectively. The cube accelerated at constant rates, and the average velocities for the slow and fast conditions were 46.3 and 57.4 cm/s respectively.

2.3. Procedures

Before the experiment began small 5 mm reflec- tive markers were placed on the thumb, index finger and wrist of the subject. To begin a trial, the index finger and thumb of the dominant hand were placed together to form a relaxed pinch which was placed over the start position. On stationary trials, the cube was held in the target zone with a 3 mm barrier that prevented the cube from rolling, and subjects were required to reach toward and pick it up whenever they were ready. The speed of these movements was self-paced. Stationary trials were performed at the two ramp inclinations asso- ciated with the fast and slow moving target speeds to ensure that the visual impact associated with the slope of the ramp did not affect the manner in which the reaches were performed. In the moving condition, once subjects were in the ready position, the experimenter released the cube at the top of the ramp. Subjects were required to grasp and lift up the cube once it arrived in the target zone, and they were allowed to initiate their movement at any time with the constraint that they do not begin moving until after the cube was released. All subjects were successful at grasping the target within the target zone. Subjects performed 10 trials of each condition and the order in which the 4 conditions were performed was randomized.

Directly above the table, focused down on the

H. Carnahan et al./Schizophrenia Research 17 (1995) 267-278 271

subject, was a Sony SVHS camera that recorded the reaching movements on videotape. These vid- eotapes were later analyzed using the Peak Performance 2-dimensional movement analysis system, which involved manually digitizing the position of the points of interest (the index finger, thumb and wrist) for each frame of tape. The Peak Performance system served to interface the video image of the limb to the digital format suitable for further computer analyses, by taking the digitized positions of the markers from the tapes, to produce -,- and v coordinates as a function of time. These coordinates described the displacement of the hand (represented by the markers). Data were sampled at 60 Hz. Displacement data were filtered at a cutoff frequency of 7 Hz using a second order dual pass Butterworth Filter. To calculate hand aperture (which reflects grasp formation) the straight line resultant distance between the index finger and thumb was determined. To derive wrist velocity, the filtered displacement data or aperture data were differentiated using the central finite differ- ence technique. A resultant value was then calcu- lated by squaring each of the x and y velocities, summing them, and taking the square root of the sum. Peak values and the time at which these peaks occurred were then picked from each curve. Typical aperture and velocity profiles are shown in Fig 2. Movement time was also calculated, and referred to the duration from when the limb lifted off the home position to when the fingers contacted the cube; it did not include the time spent generat- ing forces on the cube or lifting it up. Means and within subject standard deviations for each depen- dent measure were calculated for the 10 trials for each condition and these values were subsequently analyzed using analysis of variance (ANOVA).

Thus, means and within-subject standard devia- tions for MT, peak velocity, time to peak velocity, peak aperture, time to peak aperture and the speed of aperture closing were analyzed in separate 3 (group; LS, ULS, C) x 2 (ramp inclination; low slope and high slope) x 2 (condition; moving, sta- tionary) mixed ANOVAs, with repeated measures on the last two factors 1. ANOVA findings signifi-

llnitial analyses of covariance involving age revealed that age accounted for very little variability in any of the dependent variables. Since age had no impact on any between-group comparisons, it was dropped from subsequent analyses.

cant at p <0.05 were further analyzed using the Newman-Keuls post hoc method for comparison of means. For highest order significant findings, F ratios, means and standard error are presented.

3. Results

3.1. Movement time

In the MT analysis, there were ramp inclination by condition, F(1,20) = 41.78, p < 0.001 and group by condition, F(2,20) = 5.53, p < 0.05 interactions. As expected, when the cube was stationary, MT for the low slope was not different than the high slope. However, when the cube was moving, sub- ject's MTs were shorter when the cube was moving fastest and MT was longer when the cube was moving more slowly (see Table 2). As evident in Fig. 3, in the stationary condition the leukotom- ized group moved more slowly than the schizophre- nic and control groups, which were not different from each other. In the moving condition, the leukotomized group and control groups performed with a similar MT and both were slower than the schizophrenic group. The MT for all three groups decreased when reaching toward moving objects.

When the within-subject standard deviations of MT were analyzed there was also an inclination by condition interaction F(1,20) = 5.70, p <0.05. In the stationary condition, MT was equally vari- able for the high and low ramp inclinations. However, in the moving condition, subjects were more variable in the slow condition when com- pared to the fast.

3.2. VelociO'

Similar to the MT analysis, when peak velocity was analyzed there was an inclination by condition interaction, F(1,20) = 95.04, p < 0.01. As expected, peak velocity did not differ in the stationary condi- tion between the two ramp inclinations. But, when the target was moving, peak velocity was greater when the cube was moving rapidly.

The within-subject standard deviation analysis showed a main effect for condition, F(1,20)= 38.77, p<0,01. Subjects were more variable in

272 H.. Carnahan et aL /Schizophrenia Research 17 (1995) 267-278

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H. Carnahan et al./Schizophrenia Research 17 (1995) 267-278

Table 2 Means and standard error in parentheses for each of the four conditions (condition by ramp inclination interactions)

273

Dependent Fast moving Slow moving High Slope Low slope measure (moving) (moving) (stationary) (Stationary)

MT (ms) 523.8 (16.7) 752.9 (34.5) 813.2/29.4) 795 (27.9) PV (mm,k) 489.6 (21.7) 376.3 (22.9) 387.7 (15.9) 383.0 (18.8) TPV (mst 269.5 (12.9) 353.7 (24.3) 298.7 (14.7) 316.4 (15.7) PA (mm~ 58.8 (1.5) 51.5 (2.5) 42.6 (1.0) 41.2 (0.9) TPA (mst 372.3 (17.8) 578.9 (29.3) 621.7 (32.7) 38.1 (29.9) PAS (mm/s) 301,5 (18.1) 210,8 (16.7) 152.1 (12.9) 135.9 (8.1)

MT, moxement time; PV, peak velocity; TPV, time to peak velocity; PA, peak aperture; TPA, time to peak aperture; PAS, peak apertures speed.

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Fig. 3. Mean movement time and standard error for each of the three groups when the target was stationary and moving.

peak velocity when the target was moving (65.4 mm/s+4.1) in comparison to when it was stationary ( 33.3 mm/s + 2.8).

3.3, Time to peak velocity

For the moving target condition, peak velocity was reached sooner when the target was moving fast as opposed to moving slowly. In the stationary condition, slope inclination did not influence time to peak velocity F(1,20)=10.15, p<0.01. There

was also a group by ramp inclination interaction, F(2,20)=3.61, p<0.05. As is evident in Fig. 4, at the high ramp inclination, peak velocity was reached at a similar time by all groups. However, at the low ramp inclination peak velocity was reached later for the leukotomized group in comparison to the high ramp conditions, and in comparison to the other two groups, which do not differ from each other.

There were no statistically significant findings when the within-subject variability of the time to peak velocity was analyzed (p > 0.05 ).

274 I-1. Carnahan et aL /Schizophrenia Research 17 (1995) 267-278

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Fig. 4. Mean time to peak velocity for each of the three groups as a function o f ramp inclination.

3.4. Aperture

An inclination by condition interaction showed that when the target was moving, aperture was larger for the fast condition in comparison to the slow condition. When the target was stationary, ramp inclination did not influence aperture size, F(1,20)=16.18, p<0.01. As well, aperture size increased for both the ramp inclinations, when the targets were moving.

There was also a group by condition interaction F(2,20)=5.75, p<0.05. Fig. 5 shows that for the stationary condition, the two schizophrenic groups were not different from each other and had larger apertures than the control group. However, for the moving condition, hand aperture was smallest for the control group, intermediate for the leuko- tomized group and largest for the unleukotomized schizophrenic group. As well, aperture increased from the stationary to the moving condition for all three groups.

There was a significant group by condition inter- action when the within-subject standard deviation of peak aperture was analyzed, F(2,20)=4.05, p < 0.05. Fig. 6 shows that for the stationary condi- tion, there was equal variability for all three groups. However, when the target was moving,

there was more variability for the control group in comparison to the two patient groups which did not differ.

3.5. Time to peak aperture

In the time to peak aperture analysis there was an inclination by condition interaction that showed that ramp inclination had no influence when the target was stationary, but when it was moving, peak aperture was reached much sooner for the fast condition, F(1,20) = 48.70, p<0.01. The group by condition interaction F(2,20)=5.13, p < 0.05, showed that for the stationary condition, peak aperture was reached sooner for the schizo- phrenic and control groups, which were both different from the leukotomized group. For the moving condition, the schizophrenic group reached peak aperture sooner than either the control or leukotomized groups which were not different from each other (see Fig. 7).

For the within-subject variability analysis of time to peak velocity, there was a main effect for ramp inclination, F(1,20) = 20.31, p < 0.01. Subjects were less variable at the steep ramp inclination (70.2 ms_4.9) in comparison to the gentler inclination (120.9 ms + 12.3).

H. Carnahan et al./Schizophrenia Research 17 (1995) 267 278 275

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Fig. 6. Mean within-subject standard deviation of peak aperture for the three groups when the object was moving and stationary.

3.6. Speed o f aperture closing

An inclination by condition interaction showed that when the speed of aperture closing was exam- ined when objects were moving, aperture speed

was greater when the object was moving quickly than when it was moving slowly, F(1,20) = 27.15, p < 0.01. In the stationary condition, ramp inclina- tion did not influence rate of hand closure.

The variability of the speed of aperture closing

276 1-1. Carnahan et al./Schizophrenia Research 17 (1995) 267-278

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showed a main effect for group, F(2,20)=5.7l, p <0.05. The leukotomized group (25.0 mm/s + 3.0) was less variable than the control group (62.9 mm/s+ 13.4). The unleukotomized schizo- phrenic group was not different from either of the other two groups (42.3 mm/s+4.9).

4. Discussion

A particularly interesting finding in this study was that both the leukotomized and unleukotom- ized individuals with schizophrenia decreased their MTs in response to target movement. The leuko- tomized group decreased their MTs so that they were equal to the normal control group, and the unleukotomized schizophrenic group was actually faster than the control group. This suggests that the generalized slowing that is often reported for individuals with schizophrenia is due to impaired motor planning processes and not to any perma- nent physical or psychological constraint. In a situation where patients are exposed to a dynamic environment, the moving target helps drive the movement, and takes some of the burden of move- ment planning away from the patient (Lee, 1980). Thus, in a moving target situation, individuals

with schizophrenia can perform as fast or faster than normal control subjects.

In terms of the schizophrenic individuals' abilities to use redundant information, these data show that in the type of perceptual-motor situation evaluated in the present study, individuals with schizophrenia were very successful at using redun- dant information. The two patient groups were able to use the target movement information to speed up their movement in comparison to the static reaching conditions. They slightly overcom- pensated in response to the target movement in terms of their MTs (i.e., their MTs decreased even more than those of the controls when reaching toward the moving targets). However, this over- compensation in MT did not carry over to the kinematics. There were no group differences in the peak velocity in response to target movement, and all three groups responded similarly to the increas- ing target velocity. As well, this large decrease in MT did not affect the patients' ability to success- fully capture the cube.

It was observed that the two patient groups had larger apertures than the control subjects. However, aperture increased equally for subjects in all three groups when the target was moving. This is consistent with previous research (Wallace

H. Carnahan et al./Sehizophrenia Research 17 (1995) 267-278 277

et al., 1992) and demonstrates that the leukotom- ized and unleukotomized individuals with schizo- phrenia were responding to the target movement in a similar manner as the control subjects, again supporting the hypothesis that they are able to utilize redundant information.

In terms of our secondary aim, to compare the performance of the leukotomized and unleukotom- ized schizophrenics, there were two main findings which support the conclusion that there are deficits in fine motor control that stem from the frontal lesions of the leukotomized patients, over and above the deficits related to schizophrenia. When time to peak velocity was examined, we found that at the low ramp inclination, when the target was moving, peak velocity was reached later for the leukotomized group. Thus, for the leukotomized patients, less time in the reaching trajectory was spent decelerating toward the target in comparison to the other two groups. As well, the time to peak aperture analysis showed that less time was spent closing the hand around the object for the leuko- tomized group. Deceleration time has been previously interpreted to be an indication of the precision or fine control of a movement. Individuals use a long deceleration time when approaching small or fragile objects that require fine control, to be successfully grasped. Very short deceleration times are found when reaching toward very large or solid objects where only gross control is needed (MacKenzie et al., 1987; Marteniuk et al.. 1987). Based on this interpretation, the leukotomized group was less precise in the control of their reaching movements because they spent less time decelerating toward, and closing their hand around the object. Thus, in the present study, we were able to provide some evidence for fine motor control deficits in leukotomized patients. Since there were differences between the leukotom- ized and unleukotomized schizophrenics, this could be interpreted to indicate that the motor deficits observed in schizophrenics are not simply due to damaged frontal lobes.

For both peak aperture and the aperture closing speed there was less variability for the leukotom- ized and schizophrenic groups in comparison to the control group. While this at first may seem counter intuitive, this finding is consistent with

previous work that has examined the control of gait in the elderly. Winter (1991) has shown that some parameters of gait become more consistent with normal aging. This is actually a maladaptive strategy, as it reduces the repertoire of potential motor responses and increases the chances of instability or falls if any type of perturbation is introduced. The same sort of degenerative process could be happening in the control of grasp for the patient groups, where the schizophrenics have a reduced repertoire of motor responses.

To summarize, it appears that individuals with schizophrenia are able to use redundant informa- tion as well as controls to help control their movements. In fact, this redundant information actually facilitated the performance of their reach- ing movements. Perhaps this is because in this situation, the visual input provided by a moving target is a powerful source of information (Lee, 1980). However, future studies need to examine how healthy individuals and individuals with schizophrenia respond to situations with varying degrees of redundancy (i.e., moving toward targets with unpredictable trajectories).

Acknowledgements

This research was supported by separate NSERC research grants awarded to H.C. and D.E. Thanks to Peter Cox for his help with data collection, and to Barb Pollock for help with data analysis. A special thanks to the patients and staff at the former Westminster Campus of Victoria Hospital for their cooperation.

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