Timing and Force Control Deficits in Clumsy Children 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 va- lidity 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- 368 Journal of Cognitive Neuroscience Volume 3, Number 4 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1991.3.4.367