Develop. Med. Child Neurol. 198 1, 23, 6 11-625

Bimanual Co-ordination in Adolescent Boys with Reading Retardation

Christian Klicpera Peter H. Wolff Charles Drake

Introduction There is considerable disagreement

about the functional relationship between motor development and specific learning disabilities. The contradictory results in the clinical literature are due partly to differences in chronological age and academic deficit of the children studied, and partly to differences in the motor measures used for testing the presumed relationship. For example, elementary school children with specific learning disabilities are deficient in a broad range of neuromotor maneuvers (Fog and Fog 1963, Abercrombie et a/. 1964, Connolly and Stratton 1968) and simple motor skills (Denhoff et al. 1968, Lewis et al. 1970, Pyfer and Carlson 1972, Bruininks and Bruininks 1977), whereas learning- disabled high-school students may have no motor deficits, or deficits only in complex skills that depend on visual feedback monitoring and knowledge of results (Peters et al. 1975, Rourke 1975). The age- related dissociation between motor and cognitive impairment probably reflects a more general developmental differentia- tion between sensorimotor functions and operational thought (Piaget 1952, Satzand van Nostrand 1973).

Only some young children with learning disabilities show significant motor

impairment; many others perform at age- appropr ia te levels on conventional neuromotor measures (Denckla 1973, Mattis et al. 1975, Petrauskas and Rourke 1979). Motor impairment therefore may be characteristic of a limited subset of children with learning disability. Alterna- tively, conventional motor measures may be insensitive to subtle motor deficits or to deficits in complex motor skills, which may be characteristic of most children with learning disabilities.

For the present study, we examined the motor performance of boys with severe reading retardation, and we chose adolescence as the comparison age on the assumption that by. then sensorimotor functions and cognitive operations should be fully differentiated. We also compared three groups of severely retarded readers who were of normal psychometric intelligence but differed in subscale profiles of the standardized intelligence test.

Lashley (1951) and Bartlett (1958), among others, have emphasized the importance of temporal organization in the performance of complex motor skills. Disorders of temporal organization in motor action are also among the most sensitive markers of minor neurological impairment in infants and school-age

CorrcyonrlPnce lo Peter H . Wolff, M.D., 300 Longwood Avenue, Boston, Massachusetts 021 15.

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children (Wolff 1967, Hurwitz et al. 1972). Therefore, for this study, we selected a motor skill which emphasizes temporal organization but does not involve the potentially confounding variables of visual feedback monitoring, spatial localization or knowledge of results. Furthermore, the motor task was structured so that uni- manual and various versions of bimanual co-ordination of the same motor skill could be compared without changing the structure of the task.

Method and procedure Sample

The clinical sample comprised 30 boys aged between 11 years 5 months and 14 years 5 months (mean age 156.6 months k9 .7) who were attending a residential school for learning disabilities, who were at least lI/, years delayed in reading proficiency (mean reading retardation by Gray Oral Reading Test 34.5 months, range 18 to 70 months), but who performed in the normal range of psychometric intelligence (WISC-R mean 102.3, range 87 to 126).

The sample was preselected to include two subgroups with a discrepancy of at least 15 points on the two subscales of the WISC-R: 10 boys with relatively high verbal ( I 10 f 9) but low performance (94 t 1 I ) subscales, and nine boys with relatively low verbal (92 f 14) but high performance ( 1 13 f 13) subscales. A further subgroup consisted of I 1 boys with discrepancies of 5 points or less on the WISC-R subscales (verbal 101 f 7 , performance 103 f 10).

The control sample comprised 15 boys aged between 11 years 5 months and 14 years 5 months (mean age 157.9 monthsf9.0) enrolled in a nearby boarding school for normal students, who had no known learning disabilities or reading difficulties, who performed in the same general range of psychometric intelligence (WISC-R mean 107. 1, range 88

to 118), and all of whom had discrepancies of 5 points or less on the WISC-R subscales. Only boys who used their right hand for nine out of 10 common items from the Edinburgh Handedness Inventory were included in the study.

Method The boys tapped on two brass touch-

plates in time to a metronome beat by moving the index fingers of either or both hands at the metacarpal-carpal joint. A light touch on the plates was sufficient to generate the electronic signal for computer analysis, and there was no auditory feedback from the apparatus. The metronome, set at 92bpm, was started five seconds before and was stopped 15 seconds after the beginning of the motor trial. Subjects were informed beforehand that the metronome would be turned off, and that they should continue tapping until told to stop (45 seconds after the start of the motor trial). Their task was to maintain the training rate both before and after the metronome was turned off; and ( a ) to use either hand alone (sH); ( b ) to use both hands simultaneously (BH); (c) to alternate between the hands so that the combined motor output for the two hands equalled the expected tapping speed of92bpm (AH); and (4 to tap at the training rate of 92bpm with one (leading) hand, while the other (non-leading) hand tapped together with the leading hand on one of every three taps, and the two hands tapped in a ratio of 3.1. Practice trials were given in each mode. The order of presentations for symmetrical trials (SH, BH, AH) and for asymmetrical trials (left hand leading, right hand leading) was counterbalanced across subjects. Symmetrical trials were always administered first.

Data analysis Motor performance was recorded on

magnetic tape and analyzed by digital 618

CHRISTIAN KLICPERA PETER H. WOLFF CHARLES DRAKE

computer for: (1 ) Standard deviations from the mean of inter-tap intervals for the last 30 seconds of the motor trial after the metronome had been turned off. This value was used as the measure of tapping variability (i.e. the inverse of tapping stability). (2) Number of taps made by each hand. Absolute deviations from expected rate by each hand were used as the (inverse) measures of tapping accuracy; relative deviations were used to measure whether the subject speeded up or slowed down during a trial. (3) Performance in the asymmetric modes was further analyzed by dividing the actual tapping rate of the leading hand by that of the non-leading hand. A value of 3 .0 , was taken as the expected ratio; values less than 3 . 0 indicated that either the leading hand tapped too slowly or the non-leading hand tapped too fast.

Results Symmetrical tapping mode (SH. BH, AH)

Motor stability. A 2 X 2 X 3 repeated measures analysis of variance for group (retarded readers, normal readers), hand and mode (SH, BH, A H ) was computed on tapping variability and revealed significant main effects for group (F = 2 8 . 7 ; df = 1 3 1 ; p < O . O O l ) ; f o r h a n d ( F = 7 * 4 ; d f = 1 3 1 ; p=O.Ol ) ;andformode(F=40 .3 ; df = 2,51; p <0*001). Retarded readers tapped with greater variability of rhythm than did controls (mean 107.3 vs 5 5 . 2 , respectively). In both groups the left hand tapped with greater variability (mean 96.0) than the right (mean 83.0); and tapping was more variable in the bimanual alternating(mean 116.5) than in either the unimanual (mean 64.5) or the bimanual simultaneous mode (mean 73.0). By a posteriori comparisons of means, the significant differences across modes were between the unimanual and bimanual alternating trials (p < O * OOl), and between

bimanual simultaneous and alternating trials (p <O*OOl); but not between unimanual and bimanual simultaneous trials.

The analysis also revealed a group X mode interaction (F = 14.4; df = 2,51; p < O . O O l ) . By aposterioricomparisons of means, group differences of motor performance were significant in the bimanual alternating mode (p <O.OOl), but not in the unimanual or bimanual simultaneous mode (see Fig. 1).

Tapping accuracy. An analysis of absolute deviations from expected rate revealed a significant main effect for group (F = 6.5; df = 151; p <0.05). Retarded readers deviated more from the expected tapping rate (mean deviations /3 .5 / ) than controls (mean deviations 10.431). Hand and mode contributed no significant main or interaction effects.

In summary, the retarded readers had more difficulty than normal readers in maintaining a steady tapping rhythm, but the group differences were significant only in the bimanual alternating mode and not .in the bimanual s imultaneous or unimanual mode. The hypothesis that retarded re'aders have a selective impairment in motor tasks requiring asymmetrical timing commands to the two hands was tested further by examining subjects for tapping performance in the asymmetrical mode, with the leading hand carrying the training rate of 92bpm, and the non-leading hand tapping in synchrony on every third beat of the leading hand.

Asymmetrical tapping mode Motor stability. A repeated measures

analysis of variance for group, mode (leading hand, non-leading hand), and hand (left, right) revealed significant main effects for group ( F = 56.6; df = 132; p <0.001); and for mode (F = 84.4; df = 1,51; p < O . O O l ) , but no main or interaction effects for hand. Retarded

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I50 Retarded readers

120

60

M

SH BH AH SH BH AH

Fig. 1. Tapping variability of normal and retarded readers in symmetrical tapping modes. Ordinate = standard deviations from the mean of inter-tap intervals. SH =single hand; BH = bimanual simultaneous; AH = bimanual alternating.

readers had substantially greater difficulty tapping in a 3:1 ratio (mean variability 343- 8) than did controls (mean variability 129.0). Across groups, the non-leading hand performed with greater variability (mean 3 3 7 . 5 ) than did the leading hand (mean 135.5) . There was also a group X mode interaction ( F = 14.4; df = 1,5l; p <O. 001). By aposteriori comparisons of means, group differences were significant only in the non-leading hand (p <0*001; see also Fig. 1). The results are consistent with the hypothesis that adolescent retarded readers are specifically impaired on bimanual motor tasks requiring asymmetrical motor commands to the two hands. However, group differences in the serial organization of manual skills were limited to the non-leading hand in the asymmetrical mode and to alternating bimanual trials, when the fingers were tapping at a relatively slow speed. Thus the subject's ability to tap slowly at a controlled rate, rather than variations in central programming for bimanual synchronization, may account for group differences in the asymmetrical and synchronized alternating modes.

We therefore compared motor perform- ance across symmetrical and asymmetrical modes, with peripheral movement speed

held constant. An analysis of tapping stability in the leading hand and the same hand during unimanual performance revealed a group X mode interaction ( F = 20.5; df = 1,51; p <0*001). A similar analysis of tapping stability in the leading hand and the same hand during birnanual simultaneous performance again revealed a group X mode interaction ( F = 14.7; df= 1,51; p<O.OOl). In both comparisons retarded readers, but not normal readers, tapped with significantly greater variability of the leading hand in the asymmetrical mode (see Fig. 2), suggesting that central mechanisms of bimanual co-ordination, rather than control of peripheral movement speed, account for group differences in tapping stability.

An analysis of performance of the non- leading hand and the same hand in bimanual alternation revealed a significant main effect for mode ( F = 4 8 . 7 ; p <O.OOl). Both groups tapped with greater variability with the non-leading hand in the asymmetrical mode. In addition, there was a group x mode interaction (F= 19.4; df = 1,5l; p <O.OOl). Differences in tapping stability between the bimanual alternating mode and performance of the

iH S'H Lehng AH Non-isadlng Fig. 2. Comparison of tapping variability between symmetrical and asymmetrical tapping modes. SH =single hand; BH = bimanual simultaneous; A H = bimanual alternating. Solid lines =normal readers; dotted lines =retarded readers; Leading = leading hand in asymmetrical mode; Non-leading = non-leading hand in asymmetrical mode.

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CHRISTIAN KLICPERA PETER H. WOLFF CHARLES DRAKE

non-leading hand in the asymmetrical mode were substantially greater among retarded than among normal readers (p <0*001; see Fig. 2). Again, the results suggest that faulty mechanisms of bimanual synchronization, rather than control of peripheral movement speed, explain the group differences in motor performance. Because symmetrical trials were always administered before asym- metrical trials, we cannot exclude a transfer effect contributing to these comparisons. However, all subjects performed significantly worse on the asymmetrical trials, which were admini- stered last, so any practice effects would probably have diminished rather than exaggerated the difference between symmetrical and asymmetrical trials.

Tapping accuracy. Direct observation of the boys during performance of the asymmetrical mode indicated that retarded readers but not normal controls intermittently moved both hands simul- taneously for three or four taps in a sequence, as if they could not suppress unintended mirror movements from the leading to the non-leading hand. The observation was tested by various comparisons of tapping accuracy across groups. An analysis of absolute deviations from expected tapping rate indicated a significant main effect for group ( F = 6.5; df = I J I ; p <0.05); retarded readers deviating more from the expected rate (mean deviation /2.4/) than controls (mean deviation / I .4/). In addition, there was a group X mode interaction ( F = 9.0; df = l ,5 l ; p<0.005). By a posteriori comparisons of' means, group differences were significant i n the non-leading hand (p<O.OI). but not i n the leading hand.

Normal renders speeded up with their leading h i i d (mean 71 . O , expected rate 69.0). and at the same time slightly increased the speed of' their non-leading hand (mean 24.0. cxpected rate 23.3). so

that the correct ratio was maintained (see below). In contrast, retardedreaders tapped too fast with the non-leading hand (mean score 26.8, expected rate 23*3), but did not compensate with the leading hand (mean 70.3, expected rate 69*0), so that the correct ratio was not preserved. An analysis of the proportionate tapping rate of the leading and non-leading hands revealed a significant main effect for group (F = 13.9; df = 1 3 1; p < O * 001). Retarded readers tapped at ratios significantly below 3 - 0 (mean ratio 2-63), while normal readers preserved the correct ratio (mean 2.96).

Motor performance across ability subgroups Similar analyses, computed across the

three subgroups of retarded readers, revealed no significant main or interaction effects for ability subgroups on any outcome measure, whereas the significant main and interaction effects for mode, condition and hand for retarded readers were essentially the same as those reported in the comparison of retarded and normal readers.

Discussion Adolescent retarded. readers showed

marked impairment on a manual motor skill which requires precise temporal organization but is not materially aided by visual feedback or knowledge of results. Since the extent of motor impairment did not differ significantly across retarded readers w i t h different profiles of psychometric intelligence. this impairment may be ii general characteristic of children with specific reading retardation. and a stable chnrilctcristic of the individual whose relation with reading retardation is not obscured by developmental dif- fe re n t ia t ion or 'ni ;i t 11 r;i t io nii I c;i t c h-u p'.

Motor impairment was disclosed clearly on I y in co-ord i nit t cd hi ni;i t i ua I ski 11s. whereas the groups did not differ

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622

significantly in motor skills involving on ly one hand or the two hands in simultaneous movement. The findings are consistent with our prev ious compar i son of unimanual and bimanual performance in normal and retarded readers (Badian and Wolff 1977); and they indicate that temporal co-ordination of asymmetrical motor commands, rather than the concurrent use of the two hands or control of peripheral movement speed, was the primary source of motor deficits in retarded readers.

The performance of adult patients with surgical commissurotomy or agenesis of the corpus callosum suggests that the integrity of callosal connections is essential for the acquisition of new bimanual motor skills (Kreuter et a/. 1972, Preilowski 1972, Ferriss and Dorsen 1975, Zaidel and Sperry 1977). Callosal pathways either may regulate the corollary motor outflow that is essential for bimanual synchroniza- tion (Preilowski 1972, 1975). or they may suppress unintended mirror movements which would otherwise interfere with bimanual co-ordination (Fog and Fog 1963, Cohen 1970). However. the similar motor findings in these patients and retarded readers does not justify the conclusion that structural defects in the corpus callosum explain the impaired motor performance of retarded readers, since direct evidence for the r81e of the corpus callosum in co-ordinating bi- manual skills comes from adult patients with partial o r complete disconnections of the corpus callosum, who also suffer from significant neurological disease.

A comparison of performance on asymmetrical trials suggests that retarded readers, unlike normal controls, fail to suppress unintended mirror movements from the active (leading) to the inactive (non-leading) hand. Similar unintended mirror movements can be observed in normal kindergarten children when they

tap with one hand alone (unimanual mode) while the other hand rests on a tabletop (Wolff et a/., unpublished observation). Many children with severe learning disabilities, minor neurological impair- ment, etc., also show significantly more unintended overflow movements on neurological examination than age- matched controls (Fog and Fog 1963, Connolly and Stratton 1968). and have grea te r difficulty suppress ing such movements on command (Cohen el a/. 1967). Persistence of unintended mirror movements therefore may explain the impaired performance of retarded readers in the asymmetrical tapping mode, as well as in bimanual alternation, but should have no disruptive effect on unimanual or bimanual simultaneous performance.

At least two hypotheses can be advanced to account for the observed association between motor impairment and reading retardation in adolescence. In keeping with contemporary models of hemispheric specialization which assume that reading and serial order control of fine motor manual skills are preferentially pro- grammed from the left cerebral hemis- phere (Wyke 1967, 1971; Carmon 1971), the association between reading retarda- tion and impaired bimanual co-ordination may reflect a n underlying deficit of left hemisphere function. However, such an explana t ion leaves unanswered the question why the retarded readers of this and of a previous study by Badian and Wolff (1977) performed nearly as well as normal readers when using either hand alone or tapping in the bimanual simultaneous mode.

Since motor deficits of adolescent retarded readers were found only during co-ordinated bimanual performance, the a l te rna t ive possibil i ty remains tha t impaired mechanisms of interhemispheric communication account for both reading retardation and motor deficits. Posner

CHRISTIAN KLICPERA PETER H

et al. (1972) have proposed that reading is not exclusively a ‘left hemisphere’ task, but depends critically on neural programs from both cerebral hemispheres (see also Lassen et al. 1978). Similarly, the clinical data on adult neurological patients with callosectomies suggest that the intact corpus callosum is essential for the acquisition of synchronized bimanual skills. However, if reading retardation and impaired bimanual co-ordination have a common origin in deficits of inter- hemispheric communication, such deficits in retarded readers cannot be charac- terized simply as a failure in transcallosal transmission of information (see also Vellutino et al. 1978). Instead, they may involve a delay in transmission time or a failure to suppress unintended mirror movements to the contralateral side in complex motor skills.

In summary, the findings indicate that retarded readers are significantly impaired

WOLFF CHARLES DRAKE

on a relatively ‘pure’ manual motor task; and that complex motor skills reveal such motor deficits, even at adolescence, when they are not apparent during testing by conventional measures. Before one can conclude that impaired hemispheric co- operation is causally related to specific reading retardation, the comparison must be extended to other co-ordinated bimanual skills and to non-motoric measures of interhemispheric co-operation.

Acknowledgements: This work was supported in part by a Fogarty International Fellowship awarded to Christian Klicpera; NIMH Research Training Grant (5 T32 MH15362) and the Mental Retardation Center Core Grant (HD06276).

AUTHOR’S APPOINTMENTS Christian Klicpera, M.D. , Ph.D. , Max Planck Institute for Psychiatric Research, Munich, West Germany. Peter H. Wolff, M.D. , Children’s Hospital Medical Center, Boston. Massachusetts 02 I 15. Charles Drake, Ed.D., Landmark School, Prides Crossing, Massachusetts 01965.

SUMMARY The temporal organization of unimanual and bimanual rhythmic finger-tapping was

compared between adolesccnt normal readers and retarded readers, as well as across subgroups of retarded readers with different psychometric intelligence profiles. Regardless of subtype, the retarded readers had substantially greater difficulty in maintaining a steady tapping rhythm than did controls, but their deficit was limited to motor tasks requiring asymmetrical timing commands to the two hands. The findings indicate that the motor deficits of retarded readers on complex skills persist into adolescence; and they suggest that one major source of difficulties in motor performance may be in rapid communication between the hemispheres.

RESUME Coordination bimanuelle des garcons prisentant un retard de lecture

L’organisation temporelle de la frappe rythmique de doigt en unimanuel et bimanuel a t t t comparee entre adolescents normaux et adolescents presentant des retards de lecture mais aussi chez des sous-groupes de retard de lecture avec diffkrents profils psychomktriques d’intelligence. Quelque soit le sous-groupe, les enfants retardis pour la lecture ont prCsentt une plus grande difficultt a maintenir un rythme de frappe regulier que les contr6les mais le deficit a ktt limit6 aux tPches motrices necessitant une commande temporelle asymttrique des deux mains. Ces donnkes indiquent que les dkficits moteurs sur les tPches complexes en cas de retard de lecture persistent durant I’adolescence. Elles suggkrent qu’une source majeure de difficultks dans les performances motrices peut se situer dans la communication rap& entre les hemispheres.

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ZUSAMMENFASSUNG Bimanuelle Koordinarion bei heranwachsenden Jungen mit Leseschwache

Bei heranwachsenden Jungen mit und ohne Leseschwache, sowie innerhalb von Untergruppen leseschwacher Kinder mit verschiedenen psychometrischen Intelligenzprofilen wurde die temporale Steurung uni- und bimanueller Fingerklopfbewegungen verglichen. Unabhangig von den Untergruppen hatten die leseschwachen Kinder erheblich gro8ere Schwierigkeiten, einen gleichbleibenden Fingerklopfrhythmus aufrechtzuerhalten als die Kontrollen, jedoch war die Schwache auf motorische Aufgaben beschrankt, die zeitlich unterschiedliche Einsatze bei beiden Handen erforderten. Die Befunde deuten darauf hin, da8 die motorischen Einschrankungen leseschwacher Kinder bei komplexen Funktionen bis ins Erwachsenennalter bestehen bleiben und sie lassen vermuten, dafi ein Hauptgrund fur die Schwierigkeiten bei den Motorfunktionen moglicherweise in der raschen Kommunikation zwischen den Hemispharen zu suchen ist.

RESUMEN Coordinacidn bimanual en muchachos adolescenres con rerardo en la lectura

La organizacidn temporal del golpeteo ritmico digital unimanual o bimanual fuC comparado entre adolescentes normales y retardados para la lectura, lo mismo que en subgrupos de retrasados en lectura con perfiles psicomktricos de inteligencia diferentes. Sin atender a subtipos, 10s lectores retardados tenian una dificultad substancialmente mayor para mantener un ritmo estable continuo de golpeteo. con respecto a 10s controles, pero su deficit estaba limitado a tareas motoras que requerian la ejecuacidn asimetrica en cuanto al tiempo para ambas manos. Los hallazgos indican que 10s deficits motores de lectores retardados para abilidades complejas, persisten entrada la adolescencia; y sugieren que una importante fuente de dificultades en la realizacidn motora puede radicar en la comunicaci6n rhpida entre ambos hemisferios.

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