Timing and Force Control Deficits in Clumsy Children

Home , Athetosis, Hemiballismus, Synkinesis

Laurie Lundy-Ekman Department of Physical Therapy Pacific University

Richard Ivry Department of Psychology University of California, Santa Barbara Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/3/4/367/1754904/jocn.1991.3.4.367.pdf by guest on 18 May 2021 Steven Keele Department of Psychology University of Oregon

Marjorie Woollacott Department of Physical Education University of Oregon

Abstract This study investigated the link between cognitive processes clumsy children and the tests of timing and force. Clumsy and neural structures involved in motor control. Children iden- children with cerebellar signs were more variable when at- tified as clumsy through clinical assessment procedures were tempting to tap a series of equal intervals. They were also more tested on tasks involving movement timing, perceptual timing, variable on the time perception task, indicating a deficit in and force control. The clumsy children were divided into two motor and perceptual timing. The clumsy children with basal groups: those with soft neurological signs associated with cer- ganglia signs were unimpaired on the timing tasks. However, ebellar dysfunction and those with soft neurological signs as- they were more variable in controlling the amplitude of iso- sociated with dysfunction of the basal ganglia. A control group metric force pulses. These results support the hypothesis that of age-matched children who did not exhibit evidence of clum- the control of time and force are separate components of siness or soft neurological signs was also tested. The results coordination and that these computations are dependent on showed a double dissociation between the two groups of different neural systems.

INTRODUCTION for the hypothesis that force and timing are separate components of motor control (Keele, Ivry, & Pokorny, Component analysis allows targeted inquiries into the 1987). Moreover, the neural systems associated with relationship between the neural structures and cognitive these computations appear to be separable (Ivry & Keele, processes involved in motor control. The central tenet 1989; Ivry, Keele, & Diener, 1988; Stelmach & Wor- of component analysis is that the components of move- ringham, 1988; Stelmach, Teasdale, Phillips, & Wor- ment, defined as timing, force, and sequencing, are spec- ringham, 1989; Wing, 1988). The component analysis ified separately. Thus, regardless of whether one is framework gives rise to the hypothesis that clumsiness playing the flute or playing soccer, the timing for both may reflect different computational deficits. One form of activities would be specified by the timing component. clumsiness may reflect a deficit in timing control whereas A different component specifies force levels, again re- a different form of clumsiness may be associated with a gardless of activity. Yet another component is responsible deficit in force control. Further, given a method of iden- for sequencing of muscle activity. Research in component tifying subtle neural abnormalities, perhaps convergent analysis has focused mainly on two of these elements: information could be generated about the function of timing and force control. Studies with healthy adults and those structures. neurologically impaired subjects have provided support A method that might identify mild neural dysfunction

0 1991 Massachusetts Institute of Technology Journal of Cognitive Neuroscience Volume 3, Number 4

Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1991.3.4.367 by guest on 24 September 2021 is the use of aberrant movements, called soft neurolog- the globus pallidus. Athetotiform movements appear to ical signs. The term soft neurological signs implies that be a milder version of athetosis. the assumed etiology reflects mild forms of disorders of Synkinesis accompanies an intended movement. For the nervous system. The term soft sign contrasts with the example, while opening her mouth widely, a child may hard neurological signs used to diagnose neurological also open her eyes more widely. Or, when asked to walk disorders resulting from stroke, tumor, or degenerative on the outer soles of the foot, the arm may assume a processes. For example, strokes in the lateral cerebellar similar posture. Such movements are often associated nuclei generally produce severe dysmetria (e.g., Dich- with dyskinesias (Touwen, 1979), which are interpreted gans & Diener, 1984). Whereas hard neurological signs as basal ganglia signs. Because of this association, it has are invariably associated with a central nervous system been assumed that the neural basis of synlunesis may deficit (Tupper, 1987), soft neurological signs are more also reflect dysfunctional basal ganglia operation. difficult to define and interpret. It may be difficult to The soft signs of cerebellar dysfunction include dys-

consistently elicit these abnormalities and their appear- metria (inability to produce the correct distance for Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/3/4/367/1754904/jocn.1991.3.4.367.pdf by guest on 18 May 2021 ance may improve over time. The lack of reliability has movements), dysdiadokinesis (inability to perform rapid, led to debate in the clinical literature over whether soft alternating movements), and intention tremor (low fre- neurological signs have diagnostic value (Touwen & quency oscillation during intended movements). These Sporrel, 1979; Taylor, 1987) or can be correlated with labels are the same as used to describe the hard signs lesions of specific brain structures (Taylor, 1983). Hen- associated with cerebellar disorders, the difference being derson (1987) argues that test batteries based on soft a matter of severity. Rasmussen et al. (1983) report sta- signs are not a reliable index of brain dysfunction in tistically significant differences on tests of dysdiadoki- individual children, but that distinctions can be made nesis, dysmetria, and intention tremor between between groups of impaired and normal children (see minimally brain damaged children and age-matched con- Yule & Taylor, 1987). trols. They propose that many clumsy children can be The current study attempts to link specific, computa- classified as minimally brain damaged. tional deficits of timing and force control to soft neuro- In summary, soft neurological signs indicative of basal logical signs that are observed in clumsy children. ganglia and cerebellar dysfunction have been identified Evidence for this link would support the argument that in clumsy children or children with related disorders. there are distinct subtypes of clumsiness and attribute These studies, however, generally fail to note whether these subtypes to difficulties with distinct computations. the basal ganglia and cerebellar signs are dissociated in Moreover, the case will be strengthened that clumsiness individual children. As noted previously, the usefulness results from impairment of specific neural systems. of soft neurological signs has been questioned. The validity of this construct, especially as it applies to the study of clumsiness, would be strengthened if convergent methods were developed to link behavioral deficits to Soft Neurological Signs of Ganglia and Basal dysfunction in underlying neural systems. Cerebellar Dysfunction The basal ganglia consist of the caudate, putamen, and Experimental Tests of Force and Timing globus pallidus. In this study, the soft signs considered Control to indicate basal ganglia dysfunction are choreiform (jerky, irregular movements), athetotiform (small, slow, Evidence from a number of studies implicates the basal writhing movements), and synkinesis (type specific acti- ganglia in force control.’ Most of this research has in- vation of heterologous muscles). volved the study of patients with Parkinson’s disease, a Choreiform movements appear similar to the hard progressive disease in which the lesion focus is the sub- neurological sign of chorea. Chorea is seen in Hunting- stantia nigra of the basal ganglia. Stelmach and Wor- ton’s disease, a degenerative disorder primarily affecting ringham (1988) found that Parkinson’s patients exhibited the caudate and putamen. An animal model of chorea is irregular patterns of force development. Similar evidence exhibited after injection of biccuculline, a GABA antag- of irregular production of force pulses was seen in EMG onist, into the putamen (Crossman, Sambrook, &Jackson, records by Hallett and Khoshbin (1980). Wing (1988) has 1984). Given the similarity of choreiform movements to observed that Parkinson patients have difficulty termi- chorea, it is assumed that the former also results from nating force pulses, suggesting a more general deficit in basal ganglia dysfunction. Choreiform movements are force regulation rather than force generation. Additional often associated with developmental clumsiness (Gub- evidence for basal ganglia involvement in force control bay, 1975; Rasmussen, Gillberg, Waldenstrom, & Svenson, comes from animal studies by Horak and Anderson 1983). (1984a,b). Athetotiform movements are named for their similarity Note that the primary signs of Parkinson’s disease are to the slow, writhing movements of athetosis. Athetosis a slowing of movement and akinesia. In contrast, the is generally attributed to dysfunction of the putamen and basal ganglia soft signs reviewed above emphasize hy-

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1991.3.4.367 by guest on 24 September 2021 perkinesias, signs associated with lesions of the caudate perception of time task. On this task, subjects are pre- and putamen such as seen in Huntington’s disease. A sented with two intervals, one of a standard duration number of authors have emphasized the symbiotic re- such as 400 msec and one of a variable duration. The lationship between the different nuclei of the basal gan- subject’s task is to decide if the variable interval is longer glia, especially given that the output from these nuclei is or shorter than the standard. The duration of the variable primarily through the globus pallidus. For example, Cote interval is adjusted to determine how much shorter and and Crutcher (1985) argue that output from the striatum longer this interval must be for the subject to perform produces inhibition of the substantia nigra. If striatal at a criterion level. neurons are lost, disinhibition occurs, producing exces- Significant correlations have been obtained between sive input to the pallidus from the nigra. The result is the production and perception tests of timing control the excessive movements of chorea. Conversely, the loss (Keele et al., 1985), suggesting a common internal timing of nigral cells in Parkinson’s disease produces a reduced system. Moreover, patients with cerebellar lesions are

output from the basal ganglia. The delicate balance of impaired on both tasks in comparison to age-matched Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/3/4/367/1754904/jocn.1991.3.4.367.pdf by guest on 18 May 2021 basal ganglia activity presents a clinical challenge in the control subjects (Ivry & Keele, 1989). These results have management of Parkinson’s disease. The drugs that help led us to postulate that an important function of the them overcome their bradykinesia can end up leading cerebellum is to operate as an internal timing mechanism to a hyperkinesia. that is invoked by tasks that require precise temporal Both ends of a continuum, from akinesia to hyperki- computations (Keele & Ivry, 1991). This hypothesis de- nesia, can be interpreted as reflecting a disorder in force viates from the historical linkage of the cerebellum with control. Thus, we focus on the consistency of force pro- the motor system. The motoric role of the cerebellum duction. Rather than test the maximum force output gen- may be prominent because of the need for precise timing erated, patients or clumsy children can be tested to see in coordinated action. Nonetheless, the timing hnctions how well they can control force pulses. It is assumed of the cerebellum extend to perceptual tasks that also that, when a component process is disrupted, there will require this computation. be an increase in the variability of the computations performed by that process. Thus, the test we have de- Correlating Soft Neurological Signs and Task veloped to test force control requires the subjects to Deficits produce a series of isotonic movements to the same target (Keele et al., 1987). Initially the subject is given Previous studies of clumsy children have generally feedback so they can adjust their force pulses to match treated these children as a homogeneous group (e.g., the target. Then, isotonic movements are made without Gubbay, 1975). This approach may obscure differences feedback. The consistency of the force outpnt during this between clumsy and normal children as well as differ- phase is measured. Temporal measures such as the du- ences between subgroups of clumsy children. In the ration of the force pulses are also obtained to evaluate current study, soft neurological signs were used to divide possible trade-offs between speed and accuracy. This clumsy children into two subgroups. A clinical assess- procedure is repeated with other target forces. Parkinson ment of a population of clumsy children distinguished patients are able to maintain consistency on this task only those with soft signs associated with basal ganglia dis- by greatly reducing the speed with which they produce orders and those with soft signs indicative of cerebellar their force pulses (Ivry, unpublished data). This finding disorders. These children were then tested on experi- can be viewed as evidence of a force deficit. mental tasks that assessed force and timing control. The Our studies of timing control have also emphasized prediction was that the clumsy children with basal gan- variability measures. We have used two tasks, one for glia soft signs would have difficulty on the force control time production and one for time perception (Keele, task. In contrast, it was predicted that the clumsy children Pokorny, Corcos, & Ivry, 1985). In the production task, with cerebellar soft signs would be impaired on the the subjects attempt to produce a series of keypresses timing tasks. separated by a constant interval. A pacing signal is pro- A dissociation on the experimental tasks between vided for the first 12 responses to establish the desired subgroups of clumsy children would provide new sup- frequency such as 2 Hz. The external signal is then ter- port for a component analysis in motor control, in terms minated and the subject must rely on an internal timing of viewing force and timing control as separable com- process. The variability of the interresponse intervals putations. provides a measure of the consistency of this internal timing process. However, inconsistency at this task need RESULTS not reflect a variable timing process. The internal clock Time Production and Perception Tasks may operate properly, but the motor system may have difficulty implementing the response (Wing & Kristoffer- Tapping Task son, 1973). Thus, a second measure of timing control has A transformation was applied to the tapping data before been employed that eliminates movement demands, a performing any analyses. This transformation is standard

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1991.3.4.367 by guest on 24 September 2021 procedure and has been shown to have no effect on The implementation estimates did not differ reliably group differences. A regression line was fitted through among the three groups of subjects. the 30 intervals produced by the subject and the variability was calculated as the deviation of each response Perception Task from the regression line (see Keele et al., 1985; Ivry et al., 1988). Since our interest is in the interval-to-interval Table 2 presents the perception results. There was a variance, we do this transformation to eliminate variance significant difference between the three groups on the due to constant drift in the rate of the timing process. two tasks [F(3,32) = 3.92,p<.O3].Most interesting, there This transformation introduces a slight increase in the was a significant Group X Task interaction [F(2,32) = motor delay estimate because it decreases the positive 3.91, p<.O3]. Post hoc examination of this interaction correlation between successive responses. The total var- indicated that the children with cerebellar signs per- iability was then partitioned into clock and motor delay formed significantly poorer on the time perception task

components by the Wing and Kristofferson model (1973). than both the controls and children with basal ganglia Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/3/4/367/1754904/jocn.1991.3.4.367.pdf by guest on 18 May 2021 The covariance between successive intervals was positive signs. The control and basal ganglia groups did not differ for three of the children in the cerebellar group and one in their performance on the duration judgments. There child in the basal ganglia group. This result suggests that was no difference between the three groups on the loud- at least one of the assumptions of the Wing and Kristof- ness judgments. Thus, the perceptual deficit observed in ferson model has been violated (see also, Ivry & Keele, the clumsy children with cerebellar signs cannot be at- 1989). Thus, the tapping data for these subjects were not tributed to general factors or auditory deficits. It appears included in the following analysis. An alternative method to be selective to the ability to compare the relative for treating these violations is presented in Ivry and Keele durations of short intervals. (1989). The results are unchanged if this alternative is applied. Force Control Task Table 1 summarizes the tapping data for the control subjects and two groups of clumsy children. The mean Variability is quite large during the responses with feed- interval for all three groups is slightly faster than the back as the subjects adjust their responses to match the target interval of 550 msec. Although there are no sig- target force. Thus, the analysis focuses on the responses nificant differences in the means between any of the made without feedback. One child in the basal ganglia groups, the children with basal ganglia signs showed the group consistently pressed the response button too hard, largest speed-up. This result is similar to that reported producing a maximum value on the force transducer. in Ivry and Keele (1989) for Parkinson patients. Thus, the data for this subject were not included in the Our primary interest is in the variability of perfor- analysis of the force task. This subject was not part of the mance. There was a significant difference in the mean subset of subjects removed from the tapping analysis. standard deviation for the three groups [F(2, 30) = 5.31, The top panel of Figure 1 shows the mean force pro- p<.O2]. Post hoc analyses, conducted with the Scheffe duced at each target level for the three groups. The test, revealed that the children with cerebellar signs were relationship between standard deviation of force and significantly more variable than both the control subjects mean force produced for each target is shown in the and basal ganglia subjects. Significant differences were bottom panel of the figure. Each group graded their also obtained on the clock estimates [F(2, 30) = 3.38, responses to match the target forces. Moreover, there is p<.O5]. This effect is due to increased clock variance for a positive relationship between the mean force produced the cerebellar group in comparison to the control group. and the standard deviation. This result is in agreement There was no difference between the control group and with previous studies (Schmidt, Zelaznik, & Frank, 1979; the basal ganglia group nor was there a significant dif- Keele et al., 1987). To simplify the analysis, an average ference between the two clumsy groups on this measure. mean force and standard deviation score was calculated

Table 1. Tapping Task Scores

Group N Interval (msecj SD (mec) Clock Implementation (msec)

Control 10 532 (201 31 (8) 11 (5) Basal ganglia 10 519 (25) 37 (10) 11 (6) Cerebellar 11 541 (37) 42 (10) 14 (14)

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1991.3.4.367 by guest on 24 September 2021 Table 2. Perception Task Scores

Group N Loudness db(Aj Duration (mecj Control 10 1.60 (0.52) 52.00 (18.47) Basal ganglia 11 2.00 (1.15) 60.72 (23.92) Cerebellar 14 1.85 (0.64) 97.14 (58.54)

tasks; clumsy children with basal ganglia signs are more variable at producing force pulses. These results are in accord with the predictions outlined in the Introduction, 0 Control

where it was proposed that the basal ganglia and cere- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/3/4/367/1754904/jocn.1991.3.4.367.pdf by guest on 18 May 2021 K Cerebellar bellum are essential for force and timing computations, respectively. However, further consideration of the data leads us to believe that the double dissociation of timing and force deficits must be qualified. Force variability appears to be positively related to force and inversely related to the duration of the force pulse or correlated temporal measures (Schmidt et al., 1979;Newell & Carlton, 1988;Stel- mach et al., 1989). This suggests that it may be misleading

I I I I to examine force variability scores without reference to t 2 3 4 the kinematic features of the responses. As shown in Figure 1 and Table 3, the children with 3.0 1 cerebellar signs tended to produce smaller forces than those obtained for the other two groups. This would lead to the expectation that the variability for the cerebellar group should be lower simply because of the relationship between force and force variability. One method to correct for differences in force is to calculate a coefficient of variation, the variance divided by the mean. These values are shown in the last column of Table 3.Although there are no differences between the groups on this 1- I . I -1 It 36 44 52 60 67 75 83 91 99 measure [F(2,30) = 2.49,~<.10],the mean for the cer- Force (N) ebellar group is now higher than that obtained for the control group. Note, though, that the coefficient of variation for the basal ganglia group is still highest. Figure 1. Top panel: The relationship between mean force produced at each target level for each group of subjects. Bottom panel: Consideration of the temporal features of the force Standard deviation of produced forces as a function of the mean pro- pulses further indicates that both groups of clumsy chil- duced force for each target. dren were abnormal on the force task. The mean pulse durations were 253, 335, and 356 msec for the control, basal ganglia, and cerebellar groups, respectively. The for each subject by collapsing over the four target levels. time to peak force was approximately half these times. The means of these scores are presented in Table 3. The pulse duration means were significantly different There was no significant difference between the three from each other [F(2,30) = 3.95,~<.05],with the only groups in terms of the mean force produced. In contrast, reliable post hoc difference being between the cerebellar there was a significant difference on the standard devia- and control groups. These results suggest that the differ- tion scores [F(2,30) = 4.62,~<.02].Scheffe tests indi- ences between the clumsy groups and the control sub- cated that the group with basal ganglia signs was jects may be greater than shown in Table 3. The significantly more variable than the control group and variability scores for the control subjects should become the group with cerebellar signs. Coupled with the tap- smaller if they slowed their pulse times to approximate ping data, the results indicate a double dissociation be- those produced by the clumsy children. Since there is tween the two motor tasks and the two groups of clumsy no simple means for adjusting the variability scores to children. Clumsy children with cerebellar signs are more correct for the speed-accuracy tradeoff, additional statis- variable on the time production and time perception tics were not performed. However, given the similar

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1991.3.4.367 by guest on 24 September 2021 Table 3. Force Task Scores Group N Mean Force (newtons) SD (newtons) cv Control 10 7.3 (1.0) 1.9 (0.4) ,267 (.035) Basal ganglia 10 7.3 (1.6) 2.4 (0.4) ,336 (.090) Cerebellar 10 6.5 (1.3) 1.9 (0.4) ,303 (‘053)

temporal scores for the two clumsy groups, any adjust- Similar results were reported by Williams, Woollacott, Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/3/4/367/1754904/jocn.1991.3.4.367.pdf by guest on 18 May 2021 ment should have the same effect on both groups. Thus, and Ivry (1989) with a different group of clumsy children. even though it is ambiguous as to whether the cerebellar These findings are in accordance with the previous group is impaired on the force task, the most important results of Ivry and Keele (1989) and provide new support result from this task remains: The children with basal for our conjecture that one function of the cerebellum ganglia signs are impaired in controlling force, a finding is to operate as an internal timing system (see Keele & that stands in contrast to their normal performance on Ivry, 1991). Contrary to traditional models of the cere- the timing tasks. bellum that associate this neural system with motor or sensorimotor functions, it is postulated that the computational capabilities of the cerebellum are invoked for DISCUSSION both motor and perceptual tasks that require precise This study was designed to investigate why some children timing. are clumsy. The hypothesis was that there may be differ- Together with the timing results, the force data con- ent deficits underlying clumsiness and tested the useful- stitute a double dissociation between the two clumsy ness of a component analysis for understanding the groups and the two tasks. The children with basal ganglia subtypes of this syndrome. Clumsy children were divided signs were more variable on the force task whereas the into two groups based on the presence of different children with cerebellar signs were more variable on the classes of soft neurological signs. One group of children timing task. However, further examination of the force presented soft signs indicative of basal ganglia dysfunc- data indicates that there were differences in performance tion; the other group presented soft signs associated with between the children with cerebellar signs and the con- cerebellar disorders. The clumsy children and a group trol subjects on the force control task. The cerebellar of age-matched control subjects were tested on experi- group tended to produce smaller forces and make slower mental tasks measuring timing and force control. force pulses. Both of these differences would be ex- A consistent dissociation was found on the tests of pected to reduce variability in comparison to the control timing control. In comparison to the control subjects and subjects (Schmidt et al., 1979). Nonetheless, considera- the basal ganglia group, the children with soft cerebellar tion of the movement kinematics does not appear suffi- signs were impaired on the tapping task. The intervals cient to account for the fact that the basal ganglia group produced by the cerebellar group were more variable. was more variable than the cerebellar group. The move- In contrast, the variance scores for clumsy children ex- ment times for the basal ganglia group were close to hibiting basal ganglia signs were within normal bounds. those obtained with the cerebellar group. When the total variance was decomposed into estimates In retrospect, it is not surprising that the children with of clock and implementation components (Wing & Kris- cerebellar signs were not only more variable on the tofferson, 1973), the increased variance for the cerebellar timing task, but also performed abnormally on the force group was primarily attributed to the clock process. The task. In the force control task, each force pulse was component analysis suggests that one of the mechanisms produced in isolation and the intervals between re- underlying clumsiness in these children is an inability to sponses were randomly varied to eliminate any rhyth- control temporal parameters of movements. This hy- micity between successive pulses. In contrast, the pothesis is strengthened by the results of the perception essential feature of the timing task is the cadence. How- of time task. Only the children with soft cerebellar signs ever, timing computations may operate on different were impaired on this test. Thus, the prediction that scales. In the timing task, the scale is relatively macro- children with a movement problem would also have a scopic, i.e., across the series of responses. In the force corresponding perceptual problem was confirmed. The task, the scale may be relatively microscopic. Timing perception of loudness task supports our belief that the control may be needed to regulate the temporal rela- perceptual deficit does not reflect a nonspecific deficit, tionship between activity in agonist and antagonist mus- but reflects a specific computational disorder in timing. cles within a single pulse (Hallett, Shahani, & Young,

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1991.3.4.367 by guest on 24 September 2021 1975; Marsden, Merton, Morton, Hallett, Adam, & Rush- least when adjusted for movement time. Thus, it would ton, 1977). It is possible that the children with cerebellar appear that a balance must be achieved by the different signs are able to accurately compute the requisite force nuclei of the basal ganglia for proper force control. Dis- output for a response. However, if the onset of the an- ruption of this balance will result in increased variability tagonist muscle is delayed, the actual force produced even though the underlying mechanisms may be quite will overshoot the target. Conversely, premature onset of different. the antagonist will lead to an undershoot. Thus, increased The results of this study support the usefulness of timing variability can be expected to produce increased component analysis. Soft signs and experimental tests of force variability, even if the force computations were timing and force control provide a means for differen- perfectly normal. tiating between two different types of clumsiness. The Can a similar argument be made for an indirect effect predictions that children with basal ganglia soft signs of a force deficit on timing performance? It is possible would have force control dysfunction and children with

that someone who was irregular in force output would cerebellar soft signs would have timing difficulties were Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/3/4/367/1754904/jocn.1991.3.4.367.pdf by guest on 18 May 2021 be more variable on the tapping task because, for ex- confirmed. ample, they triggered the microswitch earlier than nor- mally desired when the force output was aberrantly large. However, the activation of the microswitch does not oc- METHOD cur at the peak force when variance is amplified, but Subjects during the rising phase of the response. The temporal effects of force variance may be negligible at this point Thirty-five 7- and 8-year-old children served as subjects. in the response. Moreover, the current results with All subjects were recruited from private schools or after- clumsy children as well as previous research with Par- school care facilities in the greater Portland, Oregon area. kinson patients (Ivy & Keele, 1989) provide empirical The clumsy children and age-matched control subjects support that people with force control deficits are not exhibited normal strength, sensation, and mentation on impaired on the tapping tasks. In addition, even if a force conventional neurologic tests. Academically, the children deficit increased variability on the tapping task, the time performed at or above grade level. None of the subjects perception task allows an independent assessment of a presented hard signs of neurological dysfunction. timing problem. Three clumsy children were referred by physical ed- The preceding arguments allow us to retain the hy- ucation teachers. The remaining clumsy children were pothesis that force and timing are separable computa- identified in a screening procedure. The screening pro- tions of coordination, presumably dependent on cedure consisted of four components: soft sign screen- different neural systems. However, there remains the ing, hard sign screening, quick screening for clumsiness, possibility that, whereas children with basal ganglia signs and the Bruininks-Oseretsky Test of Motor Proficiency are impaired at force control only, children with cere- (Bruininks, 1978). bellar signs suffer deficits in both timing and force con- The soft signs were scored according to Touwen’s trol. The current data do not allow us to differentiate (1979) criteria. All soft signs screenings were adminis- between a dual-deficit hypothesis and the hypothesis that tered by physical therapy students who did not know the a timing deficit will indirectly produce a force deficit. purpose of the experiment. The soft signs used to identify Indeed, there are atways timing and force aspects to any children as having basal ganglia involvement were chor- movement. This is one reason why the perception data eiform, athetoid, and synkinesis. To test for choreiform are so critical to the argument that the cerebellum is and athetoid movements, the child stood with feet to- essential for timing (see Ivry & Keele, 1989) since there gether, then stretched arms out front, spread fingers as are no movement requirements on these tasks. Unfor- wide as possible, closed their eyes, and stuck out their tunately, we do not have a test of force perception. tongue. This position was held, as steadily as possible, One further aspect of the force data should be noted. for 20 sec. Small, jerky movements at either distal or We have argued that force control may be dependent on proximal joints were scored as choreiform and slow, basal ganglia computations. Much of the previous human writhing movements were scored as athetoid. Synkinesis research in support of this hypothesis has been based was assessed with the child standing, feet together, and on patients with Parkinson’s disease. The children with the arms held at 90” of shoulder flexion by the examiner basal ganglia soft signs in the current study present signs providing light support at the wrist. The child was in- that are quite distinct from those observed in Parkinson’s structed to relax and allow the examiner to support the disease. The basal ganglia soft signs used as the screening arms. The child, in sequence, opened the mouth as wide procedure are hyperkinetic rather than the hypokinetic as possible, then closed eyes tightly, then stuck out the signs seen in Parkinson’s disease. Nonetheless, both the tongue as far as possible. The examiner looked for children in the current study and the Parkinson patients spreading of fingers and thumb, and wrist extension. (Stelmach & Worringham, 1988; Ivry, unpublished data) The cerebellar signs consisted of dysdiadokinesis, in- show increased variability on force control measures, at tention tremor, and dysmetria. Dysdiadokinesis was

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1991.3.4.367 by guest on 24 September 2021 tested as having the child flex one elbow to 90°, with the The child listened to computer generated pacing tones hand pointing forward. The examiner demonstrated (50 msec duration, 550 msec intervals), then synchro- three complete pronations and supinations of the wrist. nized tapping on the key with the tones. After 13 taps, The child was asked to perform this movement as fast as the tones ended and the child attempted to maintain the possible for approximately 15 sec. The examiner watched same response rate for an additional 31 self-paced taps, for smoothness of movement and movement of the el- or 30 intervals. bow. Intention tremor and dysmetria were assessed to- A block of trials ended when the subject completed gether, using two tests. The first test was the finger-to- six successful trials or four unsuccessful trials (see Ivry nose test. In the second test, the examiner held his or & Keele, 1989, for further information). Three blocks of her finger position constant and the child was asked to tapping data were obtained from each subject, yielding touch the target finger. Both tests were performed three a maximum of 18 trials for analysis. times with eyes open and three times with eyes closed. The primary measure of interest is the standard devia-

Both tests scored for tremor and for accuracy of finger tion of the interresponse intervals produced without the Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/3/4/367/1754904/jocn.1991.3.4.367.pdf by guest on 18 May 2021 placement. pacing signal. In addition this overall variability score If a child exhibited any of the soft signs, a neurological was partitioned into estimates of clock and implemen- exam of hard signs was conducted by the first author. tation variance by using a formal model developed by The children with soft signs, only, were then given a brief Wing and Kristofferson (1973). Only a brief review of screening for clumsiness with a test developed by Gub- this model will be presented; thorough discussion can bay (1978). Children with scores indicating motor prob- be found in the original paper or Wing (1980) and Ivry lems were then tested with the short form of the et al. (1988). The basic premise of the model is that the Bruininks-Oseretsky test. Physical therapy students ad- variance of the interresponse intervals is the result of ministered the Gubbay and Bruininks-Oseretsky tests. two independent sources. One source reflects variability Children were only assigned to one of the two clumsy in a central timekeeper or internal clock. This mecha- groups if they met two additional criteria: a score at or nism is assumed to determine when the desired interval below the 40th percentile on the Bruininks-Oseretsky has elapsed so that the next response can be initiated. test and at least one of the basal ganglia or cerebellar The second, independent source of variability reflects soft signs. From a total of 155 children screened, 60 noise in the execution system, that is, those processes exhibited soft signs. Twenty of these children were elim- involved in implementing the clock command that a inated from further study because they presented both movement should be made. basal ganglia and cerebellar soft signs. One child was The validity of the Wing and Kristofferson model eliminated on the hard sign screening due to reflex (1973) has been supported in a number of experiments asymmetry. Fourteen children were eliminated due to with both normal (reviewed in Wing, 1980) and neuro- Bruininks-Oseretsky scores above the 40th percentile. logical populations (see Keele & Ivry, 1988; Ivry et al., Thus, the final clumsy groups consisted of 25 children, 1988; Ivry & Keele, 1989). 11 with soft signs of basal ganglia dysfunction and 14 with cerebellar soft signs. Fourteen children without soft signs were randomly selected to serve age-matched as Perception Task! control subjects. These children were given the Bruin- inks-oseretsky test to verify that motor performance was On each trial of the time perception task, the subjects normal. Four of these subjects performed below the 40th listened to two pairs of 50 msec tones. The pairs were percentile and were eliminated. The remaining control separated by a 1-sec interval. The members of the first subjects scored above the 79th percentile. pair were always separated by a 400-msec interval. The interval between the second pair of tones was either shorter or longer than the first interval. The subjects’ task Tasks was to indicate whether the time between the second The stimuli and responses for all the experimental tasks pair of tones was shorter or longer than the time between were controlled by an Apple IIe computer. These tasks the first pair of tones. A control task was used to test for have been used in previous studies and methodological generalized deficits in auditory perception or experi- details can be found in previous reports (Keele et al., ments using psychophysical procedures. The subjects 1985, 1987; Ivry & Keele, 1989). again heard two pairs of tones. However, the interval between both pairs was always 400 msec, whereas the Time Production and Perception Tasks loudness of the second pair of tones was manipulated. The subjects judged whether the second pair of tones Tapping Tak was softer or louder than the first pair. Details of the Subjects attempted to produce a series of responses by structure of both perception tasks can be found in Ivry pressing on a microswitch interfaced with the computer. and Keele (1989).

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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1991.3.4.367 by guest on 24 September 2021 Force Control Tak equilibrium points (e.g., Stein, 1982; Bizzi & Mussa-Ivaldi, 1989). For this task, the subjects attempted to match the force exerted by the index finger to a target level. The subject’s forearm was supported, the palm was down, and the REFERENCES index finger rested atop a button attached to a force Bizzi, E., & Mussa-Ivaldi, F. A. (1989). Geometrical and me- transducer. target was represented a horizontal The by chanical issues in movement planning. In M. I. Posner line on the computer monitor. The vertical position of (Ed.), Foundations of cognitive science (pp. 769-794). the horizontal line corresponded to the amount of force Cambridge: MIT Press. the child was to generate; four vertical positions were Bruininks, R. H. (1978). Bruinink-Oseretsky Test of Motor used as targets. At the beginning of a trial, the horizontal Proficiency Circle Pines, MN: American Guidance Service. Cote, L., & Crutcher, M. D. (1985). Motor functions of the line appeared on the monitor. When a tone sounded, the basal ganglia and diseases of transmitter metabolism. In child flexed the index finger to press the button. Six E. R. Kandel & J. H. Schwartz (Eds.), Principles of neural responses with visual feedback (a vertical line which science (pp. 523-535). New York: Elsevier. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/3/4/367/1754904/jocn.1991.3.4.367.pdf by guest on 18 May 2021 indicated achieved force) and six responses without Crossman, A. H., Sambrook, M. A,, &Jackson, A. (1984). Ex- feedback were made at the target level. perimental hemichorea/hemiballismus in the monkey: Studies of intracerebral site of action in a drug-induced dys- After the last response without feedback, a 4-sec inter- kinesia. Brain, 107, 579-596. trial interval preceded the presentation of a new hori- Dichgans, J., & Diener, H. C. (1984). Clinical evidence for zontal line indicating the next target force. Each block of functional compartmentalization of the cerebellum. In the force control task consisted of three trials for each J. Bloedel,J. Dichgans, & W. Precht (Eds.), Cere6ellarfunc- of the four target forces. There were two blocks of trials. tions. Berlin: Springer-Verlag. Gubbay, S. S. (1975). me clumsy child. A study of develop- The primary measures interest were obtained from of mental apaxic and agnosic ataxia. London: W. B. Saun- the six responses without feedback. These include the ders. mean forces produced over the six responses without Gubbay, S. S. (1978). The management of developmental feedback, the standard deviation of these forces, and apraxia. Developmental Medicine and Child Neurology, 20, temporal measures of the time to peak force and the 643-646. Hallett, M., & Khoshbin, S. (1980). A physiological mechanism duration of the force pulse. of bradykinesia. Brain, 103, 301-314. Hallett, M., Shahani, B., & Young, R. (1975). EMG analysis of patients with cerebellar lesions.Journal of Neurology, Procedure Neurosurgery, and Psychiatiy, 38, 1163-1169. Children were screened individually in two sessions: The Henderson, S. E. (1987). The assessment of “clumsy”children: Old and new approaches.Journal of Child Psychol- first for strength, sensation, and mentation, and the sec- ogy and Psychiatiy, 28, 51 1-527. ond for neurological signs and clumsiness. In a third Horak, F. B., & Anderson, M. E. (1984a). Influence of globus session, subjects were individually tested on the experi- pallidus on arm movements in monkeys. I. Effects of kainic mental tasks. The order of the tasks was the same for all acid-induced lesions.Journal of Neuropbysiology,52, 290- subjects. The protocol was Tapping 1, Force 1, Tapping 304. Horak, F. B., & Anderson, M. E. (1984b). Influence of globus 2, Force 2, Time perception, Tapping 3, Loudness per- pallidus on arm movements in monkeys. 11. Effects of stim- ception. Practice was given on the tapping and force tasks ulation. Journal of Neuropbysiology, 52, 305-322. before the first block of each of these tasks. The first four Ivry, R., & Keele, S. W. (1989). Timing functions of the cere- trials of the perception tasks used extreme values for the bellum.Journal of Cognitive Neuroscience, I, 136-152. test interval or loudness to ensure that the subjects Ivry, R., Keele, S. W., & Diener, H. C. (1988). Dissociation between lateral and medial cerebellum in movement tim- understood the task. ing and movement execution. Experimental Brain Re- search, 73, 167-180. Keele, S. W., & Ivry, R. (1991). Does the cerebellum provide a Acknowledgments common computation for diverse tasks: A timing hypothe- This research was supported by grants from the Foundation sis. In A. Diamond (Ed.), Developmental and neural basis for Physical Therapy to Lundy-Ekman and an Office of Naval of higher cognitive functions. Research Contract (N00014-87-K-0279) to Keele and Ivry. Keele Keele, S. W., & Ivry, R. (1988). Modular analysis of timing in and Woollacott received support from a McDonnell-Pew Foun- motor skill. In G. Bower (Ed.), 7%epsychologyof learning dation Grant to the University of Oregon. and motivation (Vol. 21, pp. 183-228). San Diego: Aca- demic Press. Keele, S. W., Ivry, R. I., & Pokorny, R. A. (1987). Force control Note and its relation to timing. Journal of Motor Behavior, 19, 96-144. 1. The term force control is used as if it were the actual Keele, S. W., Pokorny, R. A,, Corcos, D. M., & Ivry, R. I. (1985). psychological computation. It is possible that the neural system Do perception and motor production share common tim- does not deal directly in forces, but some other variable cor- ing mechanisms: A correlational analysis. Acta Psychologica, related with force such as the setting of equilibrium points 60, 173-191. between antagonist muscles or the rate of change between Marsden, C. D., Merton, P. A,, Morton, H. B., Hallett, M., Adam,

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