Brain, Vol. 124, No. 9, 1832-1840,
September 2001
© 2001 Oxford University Press
Evidence for subcortical involvement in the visual control of human reaching
1 MRC Human Movement Group and 2 Sobell Departmentof Neurophysiology, Institute of Neurology, London, UK
Correspondence to:
Brian L. Day, MRC Human Movement Group, Sobell Department of Neurophysiology, Institute of Neurology, Queen Square, London WC1N 3BG, UK E-mail: b.day{at}ion.ucl.ac.uk
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Abstract |
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To test whether the most rapid visually evoked reach adjustments are cortically organized in humans, we have measured their latency in a healthy subject with complete agenesis of the corpus callosum. This condition precludes direct communication between left and right cerebral cortices and so, in this subject, a purely cortical visuomotor process would be expected to produce longer-latency responses to a target that appears in the visual hemifield contralateral to the responding limb (crossed) compared with the ipsilateral hemifield (uncrossed). As predicted, when performing simple reaction time tasks that involved lifting a finger or an arm in response to a visual stimulus presented to either hemifield, this acallosal subject showed a significant crossed–uncrossed latency difference (mean 35.8 ms) that was not present in control subjects (group mean 2.2 ms). In contrast, when she reached for a target that unexpectedly jumped into either visual hemifield, the latencies of mid-flight adjustment were the same (~120 ms) irrespective of either the target jump direction or which hand was used. This was not due to an early movement of the eyes bringing the target back on to the fovea since this subject's finger always deviated towards the new target position in advance of her eyes. Neither could it be explained by the use of ipsilateral corticospinal projections since transcranial magnetic stimulation over the motor cortex failed to evoke ipsilateral responses in arm or hand muscles. These results suggest that, even in humans, subcortical structures are involved in the fastest adjustments of the reaching arm made in response to fresh visual information. An additional finding in this subject was that, when reaching, the eye saccadic latency was greater by 36 ms on average when the target jumped right compared with left, irrespective of which hand was being used. This is the same value as the mean interhemispheric transfer time obtained in the simple reaction time tasks and may indicate right-hemispheric dominance for saccadic eye movement control.
callosal agenesis; subcortical; reaching; saccades; visuomotor
1DI = first dorsal interosseous; LED = light-emitting diode; TMS = transcranial magnetic stimulation
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Introduction |
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Humans, like cats, have the ability to make accurate mid-flight adjustments when reaching for a target that moves unexpectedly. In the cat these adjustments occur at remarkably short latency (70–120 ms) (Alstermark et al., 1984
) and the neural machinery responsible is thought to reside subcortically (Alstermark et al., 1987). The most rapid human reach adjustments occur at longer latency (100–160 ms) (Carlton, 1981; Soechting and Lacquaniti, 1983; Zelaznik et al., 1983; Paulignan et al., 1990, 1991; Prablanc and Martin, 1992; Day and Lyon, 2000) but nevertheless are fast compared with standard visual reaction times. Human mid-flight reach adjustments to a moving target can occur without awareness (Goodale et al., 1986; Pelisson et al., 1986; Prablanc et al., 1992) and are resistant to cognitive influence (Day and Lyon, 2000; Pisella et al., 2000). This hints at their possible subcortical organization, as in the cat, and it is noteworthy that monkeys eventually regain the ability to reach accurately for visual targets after complete removal of the striate cortex (Humphrey and Weiskrantz, 1967; Weiskrantz et al., 1977; Feinberg et al., 1978; Keating, 1980; Solomon et al., 1981). However, primates also possess major cortical networks that carry the necessary information to redirect a limb on the basis of fresh visual information (Ungerleider and Mishkin, 1982). In line with the general corticalization of function up the phylogenetic scale, such cortical networks, particularly those that engage posterior parietal areas (Desmurget et al., 1999; Pisella et al., 2000), are often considered to play the dominant, if not exclusive, role in the visual guidance of the human hand. To test whether the most rapid visually evoked reach adjustments are cortically organized in humans, we have measured their latency in a healthy subject with complete agenesis of the corpus callosum and a vestigial or absent anterior commissure. We reasoned that, if a cortical process controls the reach adjustment, then, for this subject, a left or right target jump occurring during a reach with the left or right hand should produce different latency adjustments depending upon whether interhemispheric transfer is necessary. This follows from the understanding that visual information presented in one hemifield is processed in the contralateral visual cortex and that each arm is controlled predominantly by the contralateral motor cortex. Thus, if the object jumps into one visual hemifield while the arm on the same side is being used to reach for the object, then all processing could be achieved within one hemisphere (uncrossed). Conversely, if the opposite arm were being used, then there would need to be transfer of information between the visual cortex of one hemisphere and the motor cortex of the opposite hemisphere (crossed). In a subject without a functioning corpus callosum or anterior commissure, such a transfer of information would have to be achieved via an indirect subcortical commissure. This would take more time than intracortical communication within a single hemisphere and would consequently lead to a significant crossed–uncrossed latency difference.
Crossed–uncrossed latency differences ranging from 12.4 to 61.3 ms have been reported in acallosal subjects using Poffenberger's method (Poffenberger, 1912), which employs a simple reaction time task to lateralized visual stimuli (Jeeves, 1969; Kinsbourne and Fisher, 1971; Milner, 1982; Milner et al., 1985; Clark and Zaidel, 1989). Therefore, in the present study we contrast the behaviour when performing such a reaction time task, where we expect to see a significant crossed–uncrossed latency difference in our acallosal subject, with that when reaching for a target that unpredictably jumps into either hemifield during the reach. Some of these data have been published in abstract form (Day and Brown, 2001).
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Methods |
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All procedures were carried out with the approval of the combined ethics committee of the Institute of Neurology and the National Hospital for Neurology and Neurosurgery, and informed consent was obtained according to the Declaration of Helsinki.
Acallosal subject
S.B. was an 18-year-old trainee nursery nurse who presented to one of the authors (P.B.) with tension headache. She was neurologically normal, although ambidextrous as confirmed by the Edinburgh inventory. MRI of the head showed complete agenesis of the corpus callosum, but preservation of other structures (Fig. 1). The anterior commissure was vestigial/absent (arrowed in Fig. 1) rather than demonstrating compensatory enlargement.
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Control subjects
Five young, healthy subjects recruited from departmental staff (three male, two female; age range 22–30 years; mean ± SD, 26.2 ± 3.0 years) acted as controls. Like S.B., they had no prior experience of the experimental procedures and were naive regarding the hypothesis being tested. Each control subject replicated the experimental procedures carried out by S.B. in the same order.
Cortical stimulation
Transcranial magnetic stimulation (TMS) (Magstim 200; The Magstim Company Ltd, Whitland, UK) was used to establish whether corticospinal and transcallosal projections were normal in our acallosal subject S.B. We stimulated over the hand/arm area of motor cortex using a figure-of-eight-shaped magnetic coil. EMG was recorded bilaterally from the first dorsal interosseous (1DI) and biceps brachii muscles with bipolar 9 mm diameter Ag–AgCl electrodes, bandpass-filtered at 30–1000 Hz, amplified and sampled at 2 kHz. The right or left motor cortex was stimulated at three times active motor threshold while both arms were held outstretched with the fingers fanned during stimulation. After off-line digital rectification and three-point smoothing of the EMG, 10 trials were averaged per limb with respect to the time of TMS.
Simple reaction time
For the simple reaction-time task, subjects initiated an upper limb movement using either the left or the right limb in response to a visual target appearing in the right or left hemifield (Fig. 2A).
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Subjects sat in a blacked-out room and fixated a small (2 mm diameter) red light-emitting diode (LED), which was located in the midline at the level of the nose and 50 cm in front of the eyes. The targets were two larger (2 cm diameter) yellow LEDs situated 10 cm either side of the fixation LED (11° eccentricity). A horizontal touch-plate, which detected when a body part was in contact with it, was mounted in front of the subject in the midline. For the finger extension movement, the forearm was pronated and the index finger rested on the touch-plate. For the elbow flexion movement, the forearm was semi-pronated and the ulnar surface of the clenched fist rested on the touch-plate. The beginning of a trial was indicated by the appearance of the fixation LED. A random time later (2.10–4.66 s), one of the side targets (selected pseudorandomly with equal probability) was illuminated for 1 s. Subjects were instructed to lift the designated limb rapidly from the touch-plate as soon as they detected the target's appearance. Reaction time was measured from the touch-plate output, which was sampled at 1 kHz.
Subjects were examined with this procedure for two different movements performed on two separate days. The required movement was extension of the index finger on the first day and flexion of the elbow on the second day. In both sessions, left and right sides were tested alternately in blocks of 20 trials, giving a total of eight blocks per side (total trials, 640 per subject). A trial was not included in the analysis if the reaction time was either excessively long (>3 SD above the mean) or short and anticipatory (<100 ms). The percentage of rejected trials was 1.1% for subject S.B. and varied from 0.3 to 1.4% in control subjects. A three-factor General Linear Model was applied to each subject's individual reaction-time data, with factors of limb (finger, arm), side (left, right) and target (left, right).
Reach adjustments
The same visual stimuli that were employed in the reaction-time study were used to evoke mid-flight adjustments of a reach. The one difference was that the central red fixation LED was replaced with a 2 cm diameter yellow LED (Fig. 2B
).
Subjects sat in a blacked-out room with their index fingertip resting on the touch-plate, which was mounted 39 cm in front and 15 cm below the central LED. A trial began with the illumination of the central LED. An auditory tone (1 kHz for 50 ms) was delivered 3 s later to act as a cue for the subject to reach out and touch the illuminated central target. In one-third of the trials (selected pseudorandomly), 25 ms after the finger left the touch-plate the central target was turned off and either the left or right LED (with equal probability) was turned on, giving the appearance of a jumping target. The subject was instructed to touch the illuminated target whether or not it jumped. The trajectory of the fingertip was measured in three dimensions using a motion analysis system (Selspot II; Selcom AB, Pantille, Sweden). Horizontal eye movements were measured on the electro-oculogram recorded from a pair of 9 mm diameter Ag–AgCl electrodes taped to the skin adjacent to the outer canthi of the eyes. Data were collected at 800 Hz and later averaged over every four points to improve the signal-to-noise ratio, giving an effective sampling frequency of 200 Hz.
The left and right arms were studied separately in blocked trials within the same session. This procedure was repeated on two separate days, the order of limb testing being reversed on the second day. Subjects performed 60 reaching trials with each arm in the first session and 96 trials per arm in the second session. The data from both sessions were combined to give a total of 312 reaching trials per subject.
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Results |
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Cortical stimulation
In S.B., the latency of EMG responses in the active contralateral 1DI was 19 and 20 ms following TMS over the left and right motor cortices, respectively (Fig. 3
). No transcallosal suppression of ongoing activity was seen in the ipsilateral limb (Fig. 3) at an intensity that induces clear-cut inhibition in healthy subjects (Ferbert et al., 1992). Ipsilateral corticospinal projections were not conspicuous since no short-latency facilitation was observed in active ipsilateral muscles.
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Simple reaction time
In general, S.B. had a slower reaction time (mean 320.9 ms) than control subjects (group mean ± SD, 251.9 ± 22.2 ms).
S.B. had a highly significant crossed–uncrossed latency difference for both finger extension and elbow flexion movements, as shown by a sidextarget interaction [F(1,625) = 42.34; P < 0.001]. Thus, as seen in Fig. 4, the mean reaction time was longer when the target appeared on the opposite side to the limb being used compared with when it was on the same side (finger, 349 versus 305 ms; elbow, 328 versus 301 ms). This interaction was not significant in any of the control subjects (P > 0.15 in all cases), and the mean crossed–uncrossed latency difference in the control group was only 2.2 ms compared with 35.8 ms in S.B.
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In S.B. the reaction of the elbow was significantly faster than that of the finger (mean 11.4 ms; limb main effect, F(1,625) = 3.93; P < 0.05). Significant differences between the finger extension and elbow flexion tasks were also present in three of the control subjects, but in these cases the finger was faster than the elbow (P < 0.001 in each case).
Reach adjustment latency
When the subject was reaching for the central target, lateral jumps of the target evoked rapid mid-flight adjustments of the arm in all subjects. These adjustments are clearly visible in the lateral component of finger velocity traces of averaged (Fig. 5) and single (Fig. 6) trials. Measuring from averaged traces (after subtraction of the mean unperturbed trajectory), it is evident that S.B.'s finger deviated in the direction of the target jump, with a latency of ~120 ms irrespective of which hand was used or the direction in which the target jumped (Fig. 5A). Therefore, unlike in the simple reaction-time experiments, no extra time was required for S.B. to react when the stimulus appeared in the hemifield contralateral to the side of the responding limb. S.B.'s mean reach adjustment latency was within the range of the control subjects' values (latency range, 121–154 ms; group mean ± SD, 137.5 ± 12.6 ms).
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Eye movements associated with reach adjustments
One possible explanation for S.B.'s lack of latency cost in the crossed reaching task is that the eyes may have deviated in advance of the finger in order to bring the target into the ipsilateral hemifield. However, the mean electro-oculographic traces in Fig. 5
suggest this was not the explanation as, on average, the eyes moved 
40 ms after the finger started to deviate towards the target. This was confirmed when traces were aligned to the time of eye movement in single trials. It is apparent that S.B.'s finger deviated in advance of her eyes in every perturbed trial (Fig. 6A). This was not necessarily the case for control subjects (e.g. Fig. 6B). It is also evident from Fig. 6 that the eye and hand deviations were not strictly time-locked. Thus, alignment of traces to the eye movement onset instead of to the target jump did not reduce the temporal variability of the reach adjustments.
It is worth noting that S.B.'s spontaneous saccadic eye movements to the jumping target had a consistently longer latency when the target jumped to the right compared with the left, irrespective of which hand was used (mean ± SD: target right, 215 ± 23 ms; target left, 179 ± 24 ms; P < 0.001) (Figs 5A and 6A). This behaviour was not observed in the control subjects (group mean ± SD: target right, 164 ± 14 ms; target left, 169 ± 15 ms).
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Discussion |
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According to the rationale outlined in the introduction, the absence of a crossed–uncrossed latency difference in S.B. suggests that the fastest visually evoked reach adjustment is not controlled by a purely cortical process. This implies the involvement of subcortical structures in the visuomotor process. However, first it is necessary to examine some possible violations of the underlying assumptions.
In callosal agenesis, the anterior commissure may be absent or present in varying degrees (Loeser and Alvord, 1968) but is often enlarged (Martin, 1985; Ziemann et al., 1999). This is relevant since it has been suggested that transfer of visual information can occur via the anterior commissure (Martin, 1985; Fischer et al., 1992). However, this is unlikely to have been significant in the present experiments since in S.B. the anterior commissure is absent or vestigial.
The developmental abnormality associated with callosal agenesis may lead to abnormal representations of visual space in the visual cortices such that each hemifield no longer projects exclusively to the contralateral hemisphere. This possibility seems unlikely, given that in S.B. significant crossed–uncrossed latency differences were present in simple reaction-time tasks that employed the same visual stimuli as those used in the reaching task. For the same reason, it seems unlikely that unusually strong projections from the motor cortex to ipsilateral muscles could account for the uniformity of mid-flight adjustment latencies in S.B. Furthermore, ipsilateral corticospinal projections were not conspicuous when the motor cortex was stimulated using TMS (Ziemann et al., 1999). The response to TMS in the contralateral arm was large and of normal latency, confirming that rapidly conducting pyramidal pathways to the opposite limb were intact. However, even at high stimulation intensities, there was no evidence of any projection from the motor cortex to the ipsilateral arm, or, indeed, of any transcallosally mediated inhibition of the tonic activity in this limb. Under similar test conditions in subjects with intact callosa, inhibition of ongoing EMG activity occurs about 30–60 ms after TMS in ipsilateral limb muscles (Ferbert et al., 1992).
One other potential problem is that early movement of the eyes may have either taken the displaced target out of the intended hemifield or else acted as a cue to the arm through an efference copy mechanism. However, electro-oculographic eye movement recordings showed that this was not the case. In S.B., when the target jumped laterally during a reach, the arm trajectory consistently deviated towards the target before any saccadic eye movement was initiated to the target's new position.
Therefore, the involvement of subcortical structures is strongly supported by the lack of a crossed–uncrossed latency difference in the reaching task. There is no reason for supposing that the mechanism of the short latency adjustment to a reach is unique to S.B. The latency of her response was comparable to that of control subjects with presumed intact corpus callosa, and S.B. had no other abnormalities upon neurological examination or imaging. Two broad possibilities exist. Either the whole visuomotor process is organized at a subcortical level or else the visuomotor process is distributed between communicating subcortical and cortical brain regions. The precise subcortical pathways involved in mid-flight reach adjustments will need to be established by future studies, possibly in patients with focal brain lesions. However, it is noteworthy that the primate superior colliculus receives direct retinal input (Kaas and Huerta, 1988) and also contains units that have firing patterns closely linked to upper-limb reaching movements (Werner, 1993). The cerebellum is also a structure of interest since it has been shown that ataxic patients with cerebellar damage have some movement abnormalities that are specifically related to the visual control of reaching (Day et al., 1998).
Our results are not necessarily incompatible with the suggestion that the posterior parietal cortex plays a central role in visual guidance of the hand (Desmurget et al., 1999; Pisella et al., 2000). First, it is likely that more than one process is involved in the visual control of upper limb reaching. Day and Lyon identified two such processes: one that operates at short latency (120–160 ms) and is to some extent involuntary, and a second that operates at slightly longer latency (>160 ms) and is under voluntary control (Day and Lyon, 2000). Secondly, even if we consider only the fastest of these processes, it is possible that the visuomotor process involved requires communication between subcortical structures and areas of parietal cortex.
We assume that the crossed–uncrossed latency difference in the reaction-time task represents the time required for information to travel from the cortex of one hemisphere to that of the other via a subcortical commissure. Our estimate of 36 ms is comparable to the range of values reported from other laboratories using similar methods for studying interhemispheric transfer in acallosal subjects (range 12.4–61.3 ms) (Jeeves, 1969; Kinsbourne and Fisher, 1971; Milner, 1982; Milner et al., 1985; Clark and Zaidel, 1989) or in patients following commissurotomy (range 35–96 ms) (Clark and Zaidel, 1989; Marzi et al., 1999). It is perhaps not a coincidence that in S.B. the latency of saccadic eye movements in response to left and right target jumps also differed by 36 ms on average, eye movements to the right responding more slowly than those to the left irrespective of which hand was being used. This was a serendipitous finding but one that is compatible with right-hemispheric dominance for the control of saccadic eye movements. Thus, if saccades require participation of the right cortex, interhemispheric transfer would be necessary for the eyes to follow a target that jumps into the right hemifield (which projects to the left hemisphere) but not for a target that jumps into the left hemifield. We are not aware of any other comparable eye movement studies in acallosal subjects. However, a recent fMRI study in healthy human subjects suggests a similar right-hemispheric dominance for saccade generation and spatial attention, the active area being in the right supramarginal gyrus (Perry and Zeki, 2000). Regardless of the reason for this latency difference, the observation serves to emphasize the relative independence of the saccadic eye movement system and the fast-acting visuomotor process that controls the reaching arm.
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Acknowledgements |
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We wish to thank S.B. for her kind co-operation in these experiments and Dr R. Jägger for his helpful comments on the imaging.
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References |
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Received August 14, 2000. Revised March 27, 2001. Accepted May 14, 2001.
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