Brain, Vol. 123, No. 12, 2501-2511,
December 2000
© 2000 Oxford University Press
Anterior and posterior callosal contributions to simultaneous bimanual movements of the hands and fingers
1 Center for Neuroscience, University of California at Davis, Davis, California, 2 VA Northern California Health Care System, Martinez, California and 3 Center for Cognitive Neuroscience, Dartmouth College, Hanover, New Hampshire, USA
Correspondence to:
James C. Eliassen, Department of Neuroscience, Box 1953, Brown University, Providence, RI 02912, USA E-mail: James_Eliassen{at}Brown.edu
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Abstract |
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In order to study the role of the corpus callosum in two-handed coordination we tested callosotomy subjects while they attempted to initiate simultaneous discrete movements with both hands. We observed four split-brain patients, including one pre- and post-operatively, as well as normal and epileptic control subjects. Split-brain patients made button presses that were less synchronous than either normal or epileptic controls. Although split-brain patients' average performance did not always differ from control subjects, callosotomy resulted in a 3-fold increase in the variability with which `simultaneous' movements were initiated. The one subject tested pre- and post-callosotomy showed distinct changes in movement initiation synchrony after both the anterior and the posterior stages of the surgery. These changes suggest that anterior and posterior callosal fibres may make unique contributions to bimanual synchronization, depending on whether responses are self-initiated or in reaction to a visual stimulus. This study demonstrates that neural communication across anterior and posterior fibres of the corpus callosum strongly influences the temporal precision of bimanual coordination. Specifically, callosal transmission affects the degree of bilateral synchrony with which simple simultaneous hand and finger movements are initiated.
bimanual coordination; callosotomy; interhemispheric integration
AC = anterior callosotomy; ANOVA = analysis of variance; CC = corpus callosum; PC = posterior callosotomy; RT = reaction time
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Introduction |
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Producing coordinated two-handed movements requires precise timing between the limbs. In normal control subjects, simultaneous bilateral arm movements are made with an average temporal synchrony of 0 ms and an SD of 3.5 ms (0 ± 3.5 ms) (Bartlett and White, 1965
). Subjects can lift the index fingers of the two hands with a mean synchrony of 0 ± 11.10 ms (Warrick and Turner, 1963). The precise neuroanatomical substrates supporting simple simultaneous hand and finger movements are unknown, although bilateral temporal coordination of arm movements is disrupted by partial anterior callosotomy (Preilowski, 1972). Coordination of the hands and fingers is likely to rely on communication through the corpus callosum (CC) to an even greater extent than proximal limb movements. This is because the hands and fingers are controlled mainly by the contralateral hemisphere, whereas the arms can also be controlled to a significant degree by the ipsilateral hemisphere (Gazzaniga, 1966; Gazzaniga et al., 1967; Brinkman and Kuypers, 1972, 1973).
Findings from the crossed minus uncrossed difference (CUD) paradigm (Poffenberger, 1912) also bear upon the issue of contralateral versus ipsilateral control. The CUD task is a reaction-time paradigm in which a stimulus is presented visually or tactually to one side of the body. Subjects respond with the hand on the same (uncrossed response) or the opposite (crossed response) side of the body as the stimulus. By subtracting the uncrossed response time from the crossed response, one obtains the CUD, a measure of the callosal transit time. In normal subjects, the CUD averages ~4 ms (Jeeves, 1969; Di Stefano et al., 1980; Kaluzny et al., 1994; Iacoboni and Zaidel, 1995). Complete callosotomy or callosal agenesis leads to a large increase in the CUD, ranging from 10 to 70 ms (Jeeves, 1969; Milner et al., 1985; Clarke and Zaidel, 1989; Aglioti et al., 1993). Transmission times in these patient groups reflect alternate forms of interhemispheric communication since the callosum is absent (Marzi et al., 1999). Recent studies indicate that when subjects respond bimanually with the arms or shoulders, the CUD is eliminated, although for bimanual hand responses the CUD remains above zero (Di Stefano et al., 1980). These findings are clearly consistent with the contralateral control of distal musculature (Di Stefano et al., 1980; Berlucchi et al., 1994) and suggest that distal response coordination requires callosal transmission.
The contribution of the corpus callosum to bimanual coordination is well established (Geschwind and Kaplan, 1962; Mark and Sperry, 1968), particularly the anterior fibres (Preilowski, 1972, 1975). Few distinctions, however, have been noted between anterior and posterior callosal contributions to bimanual integration. In primates (Pandya et al., 1971) and humans (DeLacoste et al., 1985), the anterior two-thirds of the callosum interconnect the frontal lobes while the posterior third links parietal, occipital and temporal sites. Lesion studies suggest unique anterior and posterior cortical roles in bimanual coordination. In humans and monkeys, damage to frontal medial wall motor areas, including the SMA (supplementary motor area), cingulate gyrus and anterior corpus callosum, causes bimanual impairments in cooperative and interdependent hand use (Brinkman, 1981, 1984; Freund and Hummelsheim, 1985; Dick et al., 1986; Schell et al., 1986; Chan and Ross, 1988; McNabb et al., 1988; Hanakita and Nishi, 1991; Halsband et al., 1993; Kazennikov et al., 1998; Stephan et al., 1999). In comparison, Wyke showed that parietal lesions cause spatial bimanual impairments in a larger proportion of patients than either frontal or temporal lesions (Wyke, 1971). Also, previous work from our laboratory with the split-brain patient V.J., whose data are also presented here, indicates that bimanual movement direction information is integrated through the posterior corpus callosum, hinting at parietal participation in bimanual coordination (Eliassen et al., 1999). Parietal involvement in bimanual coordination is in accordance with the proposal that the parietal lobes form a posterior motor centre (Fleming and Crosby, 1955; Mountcastle et al., 1975).
In this study we examine how the CC contributes to the temporal control of bimanual movements. Although callosotomy patients can make spatially uncoupled movements, such as drawing a circle and a square simultaneously (Franz et al., 1996), temporal coupling has been shown to be similar to that of normal subjects (Tuller and Kelso, 1989; Franz et al., 1996). In this study we examine the temporal synchrony of movement initiation, as opposed to the coupling of repetitive movements, by observing the initiation of discrete symmetric movements of the hands and fingers. We suggest the following hypothesis: if anterior and posterior callosal fibres coordinate distinct temporal components of bimanual movements, then anterior and posterior callosotomy should uniquely affect bimanual temporal coordination. Moreover, these effects should be consistent with the frontal and parietal bimanual capacities noted above.
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Methods |
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Subjects
We observed the timing of simple bimanually synchronized button presses of the whole hand or index finger in three groups of subjects. The performance of two control groups, normals and neurologically intact epileptic patients (epileptic controls), was compared with that of split-brain subjects. The two epileptic control subjects each elected to receive surgery for their medically intractable seizures following their initial testing visits to us. Patient S.S. had a right orbitofrontal focus resected. Patient V.J. received a two-stage callosotomy operation. Both patients were followed for several months post-surgically, allowing us to compare the effects of callosotomy with a presumed `control' lesion to an area not known for its participation in bimanual coordination. Figure 1
presents graphically the organization of the subject groups and the postoperative course of the two epileptic controls.
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Throughout the experiment the epileptic controls and split-brain patients were treated with anti-convulsants, at the doses established by their personal neurologists. These doses did not change during the period of study. After careful explanation of the procedures used in our study, informed consent was obtained from all subjects in accordance with the Declaration of Helsinki (BMJ 1991; 302: 1194) and with approval of the University of California Institutional Review Board.
Hand preference, age and sex for each subject are detailed in Table 1. The normal controls consisted of author J.C.E and three co-workers who, although familiar with neuroscience, were not aware of the specific purposes of this experiment. Handedness in the normal controls was obtained by self-report. All three chronic split-brain subjects have been tested extensively and reported elsewhere in the literature [J.W. (Volpe et al., 1982); D.R. (Baynes et al., 1992); K.O. (Lutsep et al., 1995)]. S.S. scored positive 19 on the Edinburgh Inventory (Oldfield, 1971), indicating he was right handed, and V.J. scored negative 24, indicating a strong left-hand preference.
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The callosotomy operation sometimes spares fibres of the CC. These fibres could mediate residual interhemispheric integration and bimanual coordination abilities. J.W. had MRI-verified complete callosotomy with no sparing (Gazzaniga et al., 1985
). D.R. has a few MRI-verified spared fibres in the rostrum (Baynes et al., 1992). Acute post-surgical MRIs of V.J. have been published previously (Eliassen et al., 1999), and she exhibits no evidence of interhemispheric transfer (Baynes et al., 1998). K.O. has MRI-verified sparing of the ventral middle one and a half centimetres of the callosum, which mediate some tactile interhemispheric transfer (Lutsep et al., 1995). Although K.O. performs better than J.W. and D.R. in three of the five conditions, her performance is otherwise similar. Furthermore, her performance is comparable to patient V.J. after complete callosotomy. For these reasons we think it fair to group K.O., J.W. and D.R. for statistical analysis.
Apparatus
Data were collected using two electronic timers and a button box situated on a table in front of each subject as in Fig. 2. The two electronic timers were positioned at an easy viewing distance from the subject. The button box was taped to the table and located at a comfortable distance from the subject. Another button box was held out of view by the experimenter and used to start both timers simultaneously. The subject had unrestricted vision of the two response buttons, the timers and their red light-emitting diode readouts, unless prevented by means of a barrier as described below. The timers displayed elapsed time in milliseconds and each button on the response box stopped one of the timers, the left button for the left timer and the right button for the right timer. All four normal controls and one epileptic control (S.S.) were tested in our laboratory. The other epileptic control (V.J. pre-surgically) and the three split-brain subjects were tested in their homes. Patient V.J.'s last session [post-PC (performance after posterior callosotomy)] was conducted at our facility.
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Behavioural paradigm
The experimental paradigm was divided into two parts, a reaction time section and a preferred-pace section, for a total of seven blocks of 40 trials each. The first three blocks tested unimanual and bimanual simple reaction time (RT). The last four blocks measured the synchrony of simultaneous self-paced bimanual movements of the hands and fingers. We were exclusively concerned with the temporal synchrony of discrete symmetric movement initiation of the distal limb, as opposed to continuous repetitive movements. Each trial began when the examiner pressed the start button and the light-emitting diodes began counting time. The readout of the timers served as the target visual stimulus. The subject responded by pressing the stop buttons. After each response the examiner recorded the times and reset the timers. Each trial took 5—10 s. Approximately 10 practice trials were administered before each section of the experiment (i.e. RT or preferred pace).
The RT section was administered first, as three separate blocks of 40 trials each. The order was left hand unimanual, right hand unimanual, simultaneous bimanual. Subjects held the responding hands outstretched and flat with palms down and fingers together. The buttons were contacted by the index finger or between the index and middle fingers near the distal joint of the index finger. Subjects were told not to move the individual finger(s) but to use the entire hand for response. These instructions were given with the intention of encouraging subjects to use wrist motions for response. However, physical restraints were not imposed to eliminate the possibility of finger movements as well. Subjects were tested under free viewing conditions, and looked at the timer of their choice if both were used. Only one timer was used during the unimanual RT conditions; the other was turned off. When the subject appeared to be ready, the examiner started the timers. Subjects pressed one or both buttons as quickly as possible once they observed the timers to be counting. The elapsed time was recorded as the subject's RT for that trial. No mention of synchronization was made before the bimanual RT condition. Subjects were told to concentrate on speed and not to worry about any differences in reaction times.
The synchronization section was administered after the RT section. In these blocks we were concerned with the difference in time of response between the hands. There were four distinct blocks derived by combining two response modes with two feedback conditions. For response mode, subjects used either the two index fingers or the two hands. When using the index fingers, subjects rested the heel of each hand on the tabletop and contacted the buttons only with the tip of each index finger. When subjects used their hands they held the fingers outstretched and flat as described above for the bimanual RT condition. For feedback conditions, subjects were either allowed to see their hands and the timers or prevented from doing so by means of a cardboard barrier. With vision allowed, subjects had feedback of the scene and knowledge of the results of each trial. When vision was obstructed, no feedback about performance was given. Pairing each response mode and each feedback condition produced the following four synchronization conditions: fingers/visible; hands/visible; fingers/hidden; and hands/hidden. Responses during the synchronization section were self paced. Subjects were instructed that when they responded, the movements must be simultaneous. Subjects were told to respond at their preferred pace once the timers began counting. If the timers were hidden, the examiner indicated verbally to the subject to proceed when ready.
For the initial testing visit the seven-block order was the same for all subjects: left RT, right RT, bimanual RT, fingers/visible, hands/visible, fingers/hidden, hands/hidden. This was the first and only visit for the four normal controls and three split-brain patients. In subsequent testing of V.J. and S.S., the administration of the blocks was varied due to the frequent seizures of patient V.J., which limited the amount of testing on several occasions. The order for S.S. was matched to that of V.J. S.S. and V.J. completed the RT section five times and the preferred-pace section four times following their (first) surgeries. After her second surgery, the posterior callosotomy, V.J. completed the RT section once and the preferred-pace section once, as well as two extra preferred-pace blocks, one of hands/visible and one of fingers/visible.
To establish the accuracy of simultaneous movements we measured the stop time difference between the timers. A perfect trial resulted in both counters displaying the same time. The difference score was calculated as the left-hand time minus the right-hand time, so in Fig. 2
, the difference score would be +15 ms. A positive score indicated the right-hand response preceded the left, and a negative score meant the left hand preceded the right. The bimanual RT block, by virtue of its bimanual response, also produced a difference score.
Data analysis
Difference scores
Statistical analysis of the preferred-pace difference scores was undertaken using JMP statistical software (SAS Institute, Inc., Cary, NC, USA) and proceeded as follows. Mean performance was analysed with linear regression on the entire set of raw difference scores from the three groups. Three independent variables were used including subject type (normal, epileptic-control, split), limb (finger, hand) and feedback (visible, hidden). Using O'Brien's test for heterogeneity of variance (O'Brien, 1979), we analysed the variability in difference scores, testing the effects of group (normal, epileptic-control, split), and within each group separately, we examined the effects of feedback (visible or hidden) and effector (finger or hand). Because the regression analysis indicated a significant effect of feedback on mean performance, variability was examined after normalizing each subject's scores to his or her mean for each condition. We also compared the means and variability of the two preferred-pace conditions, hands/visible and hands/hidden, with the bimanual RT difference scores. Means and variability were examined for each group using O'Brien's test for heterogeneity of variance and Welch analysis of variance (ANOVA) (Welch, 1951) for mean differences. We corrected for multiple comparisons using the Bonferroni approach, rejecting the null hypotheses only if P < 0.0167 for any test (i.e. 0.05/3). Mean and variability effects were also examined in the data of S.S. and V.J. after their surgeries. We used the Welch ANOVA to look for differences between means. The Welch ANOVA is appropriate when the variances of the two samples being compared are different.
Data analysis
RTs
Reaction times were analysed for changes in mean and variability. The RTs of all three groups were subjected to a single regression with hand (left/right), coordination (unimanual/bimanual) and subject-type (normal/epileptic-control/split) as independent variables. Post-hoc tests were performed on the unimanual and bimanual mean, and variance of S.S. and V.J. postoperatively. Means were examined with the Kruskal–Wallis rank sums test (Kruskal and Wallis, 1952), and variability was examined with O'Brien's test for heterogeneity of variance. We corrected for multiple comparisons using the Bonferroni approach, rejecting the null hypotheses only if P < 0.0167.
Data analysis
Outliers
Outlying data points were removed in a two-step process. First, those points >4 SDs from an individual's mean were removed for a total of seven, including two RT scores from D.R. Next, those points >4 SDs from each group mean were also removed (six additional points). Thus, a total of 13 scores were removed from the group data. Additionally, six difference scores were removed from the postoperative data of S.S. and one from V.J. post-AC (performance after anterior callosotomy).
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Results |
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Preferred-pace difference scores
Group
The regression analysis of preferred-pace difference scores indicated a significant whole-model effect, accounting for 12% of the variance (r2 = 0.120). There were significant main effects of subject type (P < 0.0001) and feedback (P < 0.0001), but no significant main effect of limb, or any two- or three-way interactions. The effect of feedback on performance can be seen in Fig. 3
, where close inspection indicates that each group showed lower means for the two hidden conditions than for the two visible conditions. A post-hoc contrast between normal and epileptic controls indicated no significant difference in mean performance (P > 0.10), but both normal and epileptic controls had significantly lower means than splits (both tests P < 0.0001).
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Variability differed significantly between each of the three groups. This effect can be seen in the standard deviation bars of Fig. 3
. Overall, normal control subjects synchronized their movements with a difference of 0 ± 8 ms (mean ± standard deviation). Epileptic controls were more variable than normals (–2 ± 11 ms; P < 0.0001), and callosotomy patients were more variable than epileptic controls (13 ± 44 ms; P < 0.0001). There were no significant effects of either limb or feedback on the variability within any group.
Preferred-pace difference scores
S.S. postoperative
Surgery led to significant changes in the performance of both S.S. and V.J. These changes are illustrated in Figs 4 and 5. Throughout the results we will present changes in mean performance followed by changes in variability. First, we introduce the findings for patient S.S. in the preferred-pace conditions. S.S. showed a significant overall decrease in mean performance following surgery to remove a right orbitofrontal focus (pre-op –1.6 ms; post-op –4.2 ms; P < 0.01). Postoperatively, there was no significant difference between the means for finger and hand use (finger –4.8 ms; hand –3.6 ms; P > 0.2). Also postoperatively, visual feedback had only a marginal effect on the means (visible –3.2 ms; hidden –5.1 ms; P < 0.05). For S.S., surgery cause only a marginal increase in overall variability (pre-op ±9.3 ms; post-op ±12.6 ms; P < 0.019). Postoperatively, finger responses were more variable than hand responses (hand ±11.0 ms; finger ±14.0 ms; P < 0.01), and hidden responses were more variable than visible ones (visible ±11.0 ms; hidden ±14.0 ms; P < 0.005).
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Preferred-pace difference scores
V.J. post-AC and post-PC
Patient V.J. also showed significant changes following each stage of the callosotomy surgery. Anterior callosotomy caused a significant decrease in the preferred-pace difference score means (pre-op –2.0 ms; post-AC –8.9 ms; P < 0.0001). Posterior callosotomy caused an additional, significant decrease (post-PC –31.5 ms; P < 0.0001 versus post-AC). Following AC, V.J. exhibited a only marginal difference between visible and hidden response means (post-AC visible –10.4 ms; hidden –7.3 ms; P < 0.04), whereas finger and hand responses had significantly different means (post-AC finger –11.4 ms; hand –6.4 ms; P < 0.001). Following PC, visible and hidden response means were significantly different (post-PC visible –39.7 ms; hidden –15.0 ms; P < 0.0001), but hand and finger responses did not differ in mean (post-PC hand –34.1 ms; finger –28.9 ms; P < 0.1).
Anterior callosotomy caused a significant increase in the variability of the difference scores and PC caused a further significant increase (pre-op ±8.5 ms; post-AC ±17.6 ms; P < 0.0001; post-PC ±27.1 ms; P < 0.0001 versus post-AC). Following AC, feedback did not have a significant effect on variability (visible ±16.7 ms; hidden ±18.5 ms; P < 0.1), nor did effector (finger ±17.0 ms; hand ±18.2 ms; P < 0.3). After PC, feedback did not have a significant effect on variability post-PC (visible ±26.2 ms; hidden ±28.9 ms; P > 0.4), nor did effector (hand ±25.2 ms; finger ±29.0 ms; P > 0.2).
Preferred-pace hands versus bimanual RT
The comparison between the means of the bimanual RT difference scores (bimanual RT) and the preferred-pace difference scores in the hands/hidden and hands/visible blocks (preferred pace) yielded significant results. The findings for difference score variability are shown in Fig. 4. There was no significant difference between preferred-pace and bimanual RT means for normals (preferred pace 0.45 ms; bimanual RT –0.60 ms; P < 0.07), and only a marginal difference for epileptic control subjects (preferred pace –0.53 ms; bimanual RT –2.58 ms; P < 0.04; Fig. 3). For split-brain patients the bimanual RT condition had a significantly lower mean than the preferred-pace condition (preferred-pace 16.4 ms; bimanual RT 0.13 ms; P < 0.0001).
Preoperatively, S.S.'s preferred-pace and bimanual RT means differed significantly (preferred pace 1.6 ms; bimanual RT –2.4 ms; P < 0.01), and postoperatively, the means were also significantly different (preferred pace –3.6 ms; bimanual RT –5.8 ms; P = 0.0164). For V.J., her preoperative means were not significantly different (preferred pace –2.6 ms; bimanual RT –2.8 ms; P > 0.9), but following AC, V.J.'s preferred-pace mean was significantly lower than her bimanual RT mean (preferred pace –6.4 ms; bimanual RT –1.2 ms; P < 0.0001). After PC, V.J.'s preferred-pace and bimanual RT means do not differ significantly (preferred pace –34.1 ms; bimanual RT –30.6 ms; P > 0.3).
The data on variability in the preferred-pace and bimanual RT difference scores is displayed graphically in Fig. 5. First we present the group data. There was no significant difference in variability between the preferred-pace and the bimanual RT conditions for either normal controls (preferred pace ±6.2 ms; bimanual RT ±5.4 ms; P > 0.1) or splits (preferred pace ±34.9 ms; bimanual RT ±37.4 ms; P > 0.4). For the epileptic controls, however, bimanual RT variability was significantly less than preferred-pace variability (preferred pace ±8.0 ms, bimanual RT ±5.3 ms, P < 0.01).
Preoperatively, S.S.'s preferred-pace and bimanual RT variability did not differ significantly (preferred pace ±9.1 ms; bimanual RT ±5.9 ms; P > 0.05), nor did variability differ significantly postoperatively (preferred pace ± 11.0 ms, bimanual RT ±10.3 ms; P > 0.4). Preoperatively, V.J.'s preferred pace and bimanual RT variability did not differ (preferred pace ±6.9 ms; bimanual RT ±4.8 ms; P > 0.07), but post-AC variability was significantly lower for the bimanual RT than preferred-pace differences (preferred-pace hands ±18.2 ms; bimanual RT ±12.3 ms; P < 0.0001). Following PC, preferred pace and RT variability again did not differ (preferred-pace ±25.2 ms; bimanual RT ±25.8 ms; P > 0.9).
Reaction times
The overall regression of RTs yielded a significant whole-model effect accounting for 36% of the variance (r2 = 0.360). There was a significant effect of subject type (P < 0.0001) and a marginal interaction of subject type by coordination (P < 0.05). There were no main effects of hand or coordination, or any other significant interactions. When the data were examined using dominant versus non-dominant hand in place of left and right, no significant effect of hand emerged either. Individual RTs are presented in Table 2. Normal controls had the fastest average RTs (216 ± 36 ms). Epileptic controls were significantly slower than normals (306 ± 91 ms; P < 0.0001), and callosotomy subjects were significantly slower than the epileptic controls (400 ± 168 ms; P < 0.0001). For normal control subjects, bimanual RTs were significantly faster than unimanual (bimanual 208 ms; unimanual 224 ms; P < 0.0001). For epileptic controls, bimanual RTs were significantly faster than unimanual (bimanual 294 ms; unimanual 318 ms; P < 0.013). For split-brain patients, unimanual and bimanual RTs were not significantly different (bimanual 405 ms; unimanual 395 ms; P > 0.3).
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S.S.'s focal resection led to no significant change in RT means (pre-op 326 ms; post-op 310 ms; P > 0.3). Post-operatively, S.S.'s bimanual RTs were significantly longer than unimanual (bimanual 321 ms; unimanual 299 ms; P < 0.0001). V.J.'s AC did not affect mean RT (pre-op 286 ms; post-AC 268; P > 0.2), whereas PC caused an increase in RT (post-PC 300 ms; P < 0.0001 versus post-AC). Following AC, the unimanual and bimanual RT means were not significantly different (unimanual 268 ms; bimanual 268 ms; P > 0.2), but after PC, unimanual RTs were significantly faster than bimanual (unimanual 285 ms; bimanual 314 ms; P < 0.005). Furthermore, PC led to a significant difference in RT between the hands. Left-hand RTs were significantly faster than right (left 276 ms; right 323 ms; P < 0.0001), whereas no such difference existed previously. As a final note, V.J.'s preoperative and post-PC RT means were not significantly different (pre-op 286 ms; post-PC 300 ms; P > 0.09).
For normal controls, bimanual RT variability was significantly lower than unimanual (bimanual ±28.5 ms; unimanual ±41.5 ms; P < 0.0001). For epileptic controls, unimanual and bimanual RT variability were not significantly different (bimanual ±84.2 ms; unimanual ±96.5 ms; P > 0.1), nor were they different for callosotomy patients (bimanual ±168 ms; unimanual ±169 ms; P > 0.9). In contrast to variability, the left- and right-hand RTs were significantly correlated for all groups (normals r = 0.968, P < 0.0001; epileptic controls r = 0.998, P < 0.0001; split-brain patients r = 0.957, P < 0.0001).
Right orbitofrontal resection caused a significant decrease in RT variability for S.S. (pre-op ±92.2 ms; post-op ±72.8 ms; P < 0.01). S.S.'s post-operative bimanual and unimanual variability did not differ significantly (bimanual ±70.3 ms; unimanual 73.5 ms; P > 0.6). For V.J., AC caused a large decrease in RT variability (pre-op SD ±86.4 ms; post-AC ±57.8 ms; P < 0.0001), but PC led to no significant changes (post-PC ±68.0 ms; P > 0.05 versus post-AC). Post-AC V.J.'s bimanual RT variability was marginally lower than unimanual (unimanual ±64.0 ms; bimanual ±51.0 ms; P < 0.04), but post-PC bimanual RT variability was significantly greater than unimanual (unimanual ±51.1 ms; bimanual ±78.9 ms; P < 0.001). Unlike the left- and right-hand RT means discussed above, V.J.'s post-PC left- and right-hand RT variability were not significantly different (left ±60.0 ms; right ±67.8 ms; P > 0.3).
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Summary and discussion |
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Our results indicate that the corpus callosum is necessary to synchronize precisely the initiation of two-handed movements. Callosotomy reduces the precision of simultaneous movements in terms of both mean and variability (Figs 3 and 4
). In contrast, a `control' focal resection of right-orbitofrontal cortex, although inducing a significant negative shift in mean response time differences, only causes a marginal increase in variability. The differences in performance between normals and epileptic controls likely result from the combined effects of age, epilepsy, anti-convulsant medication and possible familiarity with the experimental purpose. In contrast, the differences between epileptic controls and the split-brain subjects result largely from callosotomy. The callosotomy surgery alters bimanual temporal coordination in ways that a focal lesion to right orbitofrontal cortex does not.
Our findings extend to movements of the hands and fingers the conclusion that the production of temporally interdependent arm movements requires the anterior callosum (Preilowski, 1972). Although this fine temporal precision deteriorates following callosotomy, other studies suggest that movements can be coupled normally following callosotomy (Ettlinger and Morton, 1963; Tuller and Kelso, 1989; Franz et al., 1996). Moreover, even these data indicate significant correlation between bimanual RT responses. At least three possible mechanisms might support movement coupling. First, the anterior commissure or the various subcortical commissures may be involved (Mark and Sperry, 1968). Secondly, ipsilateral control mechanisms, as discussed in the introduction, might influence movement coordination timing. Thirdly, the presence of an environmental stimulus, as in Tuller and Kelso's experiment (Tuller and Kelso, 1989) and our RT condition, might invoke attentional resources in the superior colliculi which could communicate via the collicular commissure (Sprague, 1991). These alternative pathways may explain the presence of movement coupling and RT correlation in callosotomy subjects.
This study also indicates that the posterior corpus callosum participates in temporal bimanual coordination. With only the posterior callosum intact, V.J.'s preferred-pace hand responses were significantly less synchronous in terms of both mean and variability than bimanual RT responses. One possibility is that the anterior and posterior callosum integrate different types of temporal information. In fact, the topography of callosal projections differs from rostral to caudal (Pandya et al., 1971; DeLacoste et al., 1985), and anterior and PC distinctly affect interhemispheric integration. Visual and visuo-spatial integration is disrupted by PC (Gazzaniga and Freedman, 1973; Sidtis et al., 1981; Volpe et al., 1982; Risse et al., 1989; Eliassen et al., 1999; Marzi et al., 1999), whereas movement timing coordination is primarily altered by AC (Preilowski, 1972, 1975; Eliassen et al., 1999). We speculate that the anterior callosum coordinates movement timing in relation to self-referential cues (e.g. what the other hand is doing), whereas the posterior callosum coordinates movement timing in reference to external cues (e.g. visual information).
Previous studies show that the SMA, which is interhemispherically connected via the anterior callosum, is activated by self-paced bimanual tapping (Stephan et al., 1999) and internally guided movements (Roland et al., 1980; Passingham, 1993). Also, lesions to mesial frontal cortex (e.g. SMA) impair self-initiated movements (Kazennikov et al., 1998) and the generation of cooperative movements (Brinkman, 1981, 1984). On the other hand, the posterior callosum interconnects the parietal, temporal and occipital lobes, which contain all the primary sensory cortices as well as visuospatial association areas (Andersen, 1987). During RT responses, movement is necessarily yoked to an external stimulus. Visuospatial processing mechanisms invoked under these circumstances could be integrated via the posterior callosum. Control subjects then would be predicted to demonstrate a synchrony advantage for bimanual RT responses compared with self-initiated movements. Epileptic controls, but not normals, exhibit this pattern. Normal subjects show the right relationship, though not significantly. Our sample size may have been too small, or normal controls may be at a floor in performance. Previous studies report contradictory conclusions regarding this point. Paillard (Paillard, 1948) reports that variability is less with reactive responses than voluntary ones, whereas Bartlett and White report no difference (Bartlett and White, 1965). Yet the presence of a residual coordination advantage for bimanual RT responses following AC suggests that the posterior callosal fibres can convey temporal information with characteristics distinct from that transmitted across the anterior callosum.
Two closing points are worthy of mention. First, these data indicate that visual feedback, as available in this task, did not significantly reduce either the mean or variability of response time differences. Secondly, our data do not establish a clear relationship between unimanual and bimanual RT means and variability. Kaluzny and colleagues have suggested that the corpus callosum is responsible for reduced bimanual compared with unimanual RT variability (Kaluzny et al., 1994). The individual data in Table 2 seem to support this conclusion, while the group data do not. Furthermore, the RT data are confounded by two problems. First, bimanual RT blocks were administered after unimanual blocks, thus lower bimanual variability and means may arise from practice. The lower mean RTs may also provide less of an opportunity for RT differences to occur. Secondly, two stimuli, the timers, were used in the bimanual condition, but only one during the unimanual. These limitations notwithstanding, callosotomy clearly impairs bilateral motor integration.
Recent studies of bimanual integration (Donchin et al., 1998; Andres et al., 1999) have attempted to determine the neurophysiological mechanisms of bimanual control. Possible mechanisms include interhemispherically synchronized activity (Murthy and Fetz, 1996) or coordinated population vector codes (Donchin et al., 1999). Our data cannot identify particular mechanisms. They can, however, suggest that searches for such activity should perhaps include simultaneous observation of both hemispheres in areas with identified bimanual functions, such as M1 (primary motorcortex) (Donchin et al., 1998), the SMA (Kermadi et al., 1998) and the parietal lobes (Marzi et al., 1999).
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We wish to thank V.J. and her husband, as well as S.S. and his wife for their patience and cooperation in the collection of the data presented here. We also thank Dr Richard Ivry for critical comments on the manuscript. We wish to acknowledge the support of the McDonnell-Pew Program in Cognitive Neuroscience and NINDS P01 NS 17778 to the University of California at Davis.
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Received July 16, 1999. Revised May 24, 2000. Second revision on August 14, 2000. Accepted August 24, 2000.
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