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1 Perception and Motor Systems Laboratory, University of Queensland, Australia
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School of Kinesiology, Simon Fraser University, Canada
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Human Motor Control Laboratory, University of Auckland, New Zealand
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Abstract |
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(Received 27 May 2004;
accepted after revision 25 August 2004;
first published online 26 August 2004)
Corresponding author R. G. Carson: Perception and Motor Systems Laboratory, Connell Building (26), University of Queensland, Brisbane, Queensland 4072, Australia. Email: richard{at}hms.uq.edu.au
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Introduction |
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It is well established that sustained voluntary contractions of the muscles on one side of the body lead to increases in the excitability of the contralateral homologous motor pathways (e.g. Cernácek, 1961). Recent studies have demonstrated that responses evoked in the musculature of the hand, by transcranial magnetic stimulation (TMS) of the motor cortex, are facilitated by tonic contraction of homologous muscles of the opposite limb (e.g. Hortobágyi et al. 2003). In the context of bimanual movements, such crossed facilitation should favour patterns of rhythmic coordination in which homologous muscles are engaged simultaneously, and disrupt those in which homologous muscles are activated in an alternating fashion.
The precise mechanisms of crossed facilitation remain a matter of debate. The finding that the potentiation of cortically elicited motor responses, during forceful contractions of the opposite hand, is preserved in patients with agenesis of the corpus callosum, suggests that at least some of the spread of excitation takes place at a subcortical level (Meyer et al. 1995). Furthermore, the elevation of motor-evoked potentials (MEPs), observed in an above elbow amputee when the muscles of the opposite phantom hand were contracted, indicates that afferent input from the muscle is not necessarily required for crossed facilitation to occur (Hess et al. 1986). It has long been known that a small proportion of corticofugal fibres do not cross at the pyramidal decussation, but project instead to ipsilateral spinal motoneurones (e.g. Phillips & Porter, 1964). To the extent that the descending commands transmitted via the crossed and uncrossed fibres are not differentiated, this organization may provide one basis for interaction between the limbs. It has also been suggested that patients with overt mirror movements (e.g. Farmer et al. 1990) represent an extreme end of a spectrum of contralateral activation due to branched bilateral corticomotoneuronal projections, which is expressed in varying degrees in all individuals (Chiappa et al. 1991). Nonetheless, it is also likely that the coupling between the hands is mediated, at least in part, by the fibres of the corpus callosum (e.g. Geschwind & Kaplan, 1962; Mark & Sperry, 1968).
That which remains unresolved is the extent to which these various mechanisms may be implicated in mediating the interactions between the limbs which govern the stability of bimanual coordination. The present study was designed to investigate this issue, by examining the changes in excitability in human forearm corticospinal projections and spinal reflex pathways that occur during rhythmic voluntary movements of the opposite limb.
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Methods |
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Thirty normal male and female volunteers (22–38 years) participated in 40 experiments. The procedures were performed in accordance with the guidelines contained in the Declaration of Helsinski, and were approved by the Medical Research Ethics Committee of the University of Queensland. Each person provided informed consent prior to his or her participation in the study.
Apparatus
The participants were seated in a comfortable chair that provided support for the head, neck, and torso. The forearms were supported and stabilized in a neutral (semiprone) position. The elbows were semiflexed (100 to 120 deg), and the upper arms restrained against the torso. The hands were secured in manipulanda that were mounted on rotating shafts located coaxially with the axes of rotation of the wrists. Potentiometers coupled to these shafts transduced displacements of the wrists in flexion–extension. The manipulanda fixated the hands at mid palm, obviating the activation of the long finger flexor muscles that might arise from the formation of a grasp. The coupling between the manipulandum and the rotating shafts accommodated any small change in the centre of rotation of the joint that might occur during flexion and extension of the wrist. The manipulanda were made of light alloy, of very low inertia and virtually free of friction. In some experiments, the shaft of the right manipulandum was fixed with the wrist in a neutral position. In experiments in which stretch reflexes were elicited, displacements of the right wrist were induced by an AC servo motor (Baldor BSM 4250AA, Fort Smith, AR, USA). Auditory signals providing pacing for movements of the left wrist (two per movement cycle) were presented via speakers placed behind the participants. These consisted of a tone presented to the right of the participant (50 ms sine wave (540 Hz)), and a discernibly different tone presented to the left of the participant (50 ms square wave (555 Hz)). The tones were generated by a custom I/O board driven by a microcomputer.
Electromyographic recordings
The electromyographic (EMG) activity of flexor carpi radialis (FCR), and extensor carpi radialis longus (ECR) was recorded from both arms using bipolar surface electrodes. EMG signals were amplified and bandpass (30 Hz–1 kHz) filtered (Grass P511 amplifier, Astro-Medical, West Warwick, RI, USA). These signals were digitized at an analog–to–digital interface at a sampling rate of 2000 Hz. In experiments in which f-waves were elicited, the EMG recordings from the right FCR were obtained using fine wire (75 µm) bipolar hook electrodes, inserted into the muscle via 27 gauge needles. The needles were removed prior to recording. Each wire was inserted separately, with a spacing of approximately 5 mm.
Transcranial magnetic stimulation
Magnetic stimuli were delivered to the motor cortex by a Magstim 200 stimulator (Magstim, Whitland, Dyfed, UK), using a figure of eight coil (o.d. of each half-coil, 55 mm), located at the optimal position to evoke a short-latency response in the FCR muscle of the right arm. The stimulating coil was orientated so that the axis of intersection between the two loops was orientated at approximately 45 deg to the sagittal plane. It was anticipated that this arrangement would induce posterior to anterior current flow across the motor strip in the primary motor cortex. The optimal position for eliciting MEPs in the contralateral FCR was established and marked directly on the scalp. The lowest stimulation intensity at which potentials of peak-to-peak amplitude of approximately 50 µV were evoked in at least three out of five trials was taken as the passive threshold. The level of stimulation used during each experimental trial was 115% of the passive threshold. At these intensities, a potential was also evoked in ECR. Care was taken to ensure that the coil was held at the correct position on the scalp before each trial, by verifying that stimulation at the passive threshold evoked a small (
50 µV) response in FCR.
Cervicomedullary stimulation
Stimulation of the cervicomedullary junction (Ugawa et al. 1991) was carried out by passing an electrical pulse (50 µs square wave, D180A stimulator, Digitimer Ltd, Welwyn Garden City, Herts, UK) between Ag–AgCl surface electrodes filled with conductive gel, which were fixed over the mastoid processes. The stimulus intensity was varied between 30 and 50% of stimulator output (450–700 V), to produce compound motor action potentials of at least 100 µV in the right FCR.
Peripheral nerve stimulation
Stimuli were delivered by an isolated stimulator (Grass S88, Astro-Medical, West Warwick, RI, USA or Digitimer DS7A). H-reflexes were elicited in right FCR by stimulating (1 ms square wave) the median nerve at the cubital space. Stimulus intensities were adjusted to produce a clearly defined H-wave in association with a small m-wave (10% maximum). Care was taken to ensure that responses were evoked on the ascending limb of the stimulus–response curve. F-waves were elicited in right FCR by stimulating (500 µs square wave) the median nerve at an intensity at least 30% greater than that necessary to obtain a maximum m-wave.
Stretch reflexes
A servo control system (dSPACE, Paderborn, Germany) was programmed to generate the stretch stimulus. This consisted of 20 deg extension of the right wrist from a neutral starting position (50 ms duration), followed immediately by 20 deg flexion (50 ms duration). At the conclusion of the stimulus (100 ms duration), the wrist was thus restored to the neutral position. The participants were instructed not to contract the muscles of the right arm during the experimental trials, nor to react to the stretch stimuli. The experimenter monitored EMG activity in the muscles of the right arm via an on-line visual display. Only individuals for whom it was possible to obtain a stretch reflex response consisting of two distinct components, when the muscles were otherwise quiescent, participated in these experiments.
Procedure
The participants produced rhythmic flexion and extension movements of the left wrist, at a frequency of 2 Hz, in time with the auditory metronome (two beats per movement cycle). Each trial (66 s duration) commenced with the wrist in a neutral position. The participants were instructed to coordinate maximum flexion of the wrist with the sine wave tone (the first beat), and maximum extension of the wrist with the square wave tone (the second beat).
Prior to the start of each trial, a sequence of stimulus onset times was generated by computer. The interval between successive stimuli was required to be greater than 4 s and less than 12 s (mean interval 8 s). The period between successive metronome cycles was divided into eight subintervals of 62.5 ms duration. The stimulus sequence was constrained such that during the course of each trial, a single stimulus was delivered during each subinterval. There was random variation between trials in terms of the order in which stimuli were delivered during each subinterval. Following the completion of the experiment, a peak-picking routine was used to establish, on the basis of the kinematic record of the displacement of the left wrist, the time of peak flexion during each movement cycle. The movement period thus defined was divided into eight subintervals (phases) of equal duration (62.5 ms). On this basis, each evoked response was classified in terms of the precise phase of the movement cycle in which the stimulus was delivered.
In the experiments in which TMS-evoked responses, h-reflexes, and f-waves were elicited, a total of 12 experimental trials were performed in two blocks of six. In experiments in which stretch–reflexes were obtained, five trials were performed in each of four blocks, and in experiments involving transmastoid stimulation, a single block of 10 trials was performed. Control trials, in which stimuli were delivered while the left wrist was in a static neutral position, were conducted prior to and following each block of experimental trials. In obtaining summary statistics for each participant, the amplitudes of individual responses were measured and these values averaged. During the course of each experimental trial, auditory feedback of the EMG activity (amplified at high gain) of the FCR muscle of the static right arm was provided to the participants, and the levels of EMG activity in the muscles of the right FCR and ECR were monitored visually by the experimenters to ensure that the muscles were silent. Following the completion of the experiment, the root mean square (r.m.s.) amplitude of EMG activity in the muscles of the right (target) arm in the period 13–3 ms prior to the delivery of each stimulus was obtained. Relaxation in the right FCR was defined as the absence of r.m.s. EMG activity exceeding a background level of 25 µV. We also verified that there was no consistent variation in the EMG activity in the muscles of the right limb as a function the phase of movement of the opposite arm.
The magnitudes of the responses elicited during each phase of movement of the opposite arm were normalized with respect to the mean magnitude of the responses obtained during the control trials. In order to establish whether these responses differed reliably from those elicited during the static controls, means and 95% confidence intervals (n = 8 participants) were calculated for each dependent measure. The responses were deemed to have differed reliably from controls in those instances in which the value 1 (corresponding to the normalized magnitude of the control response) did not lie within the confidence interval defined by the distribution of the responses obtained for each movement phase. As a method of determining whether response magnitudes were modulated across the eight phases of the movement cycle of the opposite arm, repeated measures analyses of variance were conducted separately for each dependent measure, and post hoc contrasts (Fisher least significant difference test) employed in circumstances in which there was a main effect for phase. As a means of estimating the proportion of the overall variance accounted for by a main effect for phase, omega squared statistics were calculated following the method of Winer (1962). In order to further assist in the interpretation of the tests of significance, measures of effect size were calculated following the method of Cohen (1969). The effect size index for ANOVA (f) is a dimensionless index, which describes the degree of departure from no effect, in other words, the degree to which the phenomenon is manifested. A small effect size is considered by convention to be indicated by an f value of 0.1, a medium effect size by an f value of 0.25, and a large effect size by an f value of 0.4 (Cohen, 1969).
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Results |
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The period of each movement cycle was divided into eight phases of equal duration, for which the r.m.s amplitude of the EMG was calculated. The values obtained from all cycles within a single trial were averaged together to provide an overall representation of the patterns of muscle activation associated with performance of the task (Fig. 1). It was readily apparent that the level of engagement of the left FCR muscle was modulated markedly during the movement cycle (Fig. 1B), with the highest levels of activation occurring during phases 4, 5 and 6. A reciprocal pattern of activation was observed for the left ECR muscle (Fig. 1C).
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Motor-evoked potentials
The amplitude (peak-to-peak) and the integrated EMG (i.e. the area under the full-wave rectified curve) were calculated in the interval of the short latency response to TMS. As our analyses revealed that the pattern of variation of the two measures was essentially equivalent, we report only the response amplitudes. As Fig. 2A and Fig. 3 illustrate, during rhythmic movement of the opposite limb, the MEPs elicited from right FCR were larger than those obtained when the left arm was static. This effect was expressed reliably (P < 0.05) during phases 4, 5, 6, 7 and 8. There was a further pattern of variation that was reflected in a main effect for movement phase (F1,7 = 2.48, P < 0.05, f = 0.52, 
2 = 0.15). The MEPs recorded during phase 5 were larger than those obtained during phases 1, 2, 3, 7 and 8 (P < 0.05). A complementary pattern of results was obtained for the right ECR, although the degree of potentiation was slightly more variable across participants than that present for FCR. In conditions in which the opposite limb was moving, the mean amplitude of the FCR MEP (averaged across participants) was 0.27 mV. In the control condition, in which the opposite limb was at rest, the mean amplitude of the FCR MEP was 0.20 mV.
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2 = 0.03), and in all instances the response amplitudes could not be distinguished reliably from those obtained during the control trials. In conditions in which the opposite limb was moving, the mean amplitude of the cervicomedullary junction response (cervicomedullary-evoked potentials, CMEPs) (averaged across participants) was 0.23 mV. In the control condition, in which the opposite limb was at rest, the mean amplitude of the CMEPs was 0.24 mV. H-reflexes and f-waves
During movements of the opposite (left) limb, there was a large overall depression (P < 0.01) of the amplitude of the H-reflex elicited in right FCR, relative to resting control conditions (Figs 4A and 5). Furthermore, the extent of this depression was not constant throughout the movement cycle. Specifically, there was less depression of the H-reflex during phases 5, 6 and 7. This modulation was expressed as a main effect for movement phase (F1,7 = 3.84, P < 0.05, f = 0.65, 2 = 0.26). The responses recorded during phase 6 were larger than those obtained during phases 1, 2, 3, 4 and 8 (P < 0.05). In addition, responses elicited during phases 6 and 7 were larger than those recorded during phases 2 and 3 (P < 0.05). We also verified that an equivalent pattern of variation was obtained when the amplitude of each H-wave was expressed as a ratio of the corresponding m-wave response (F1,7 = 2.69, P < 0.05, f = 0.54). In conditions in which the opposite limb was moving, the mean amplitude of the H-reflex (averaged across participants) was 1.04 mV, and the mean amplitude of the corresponding m-wave was 0.85 mV. In the control condition, in which the opposite limb was at rest, the mean amplitude of the H-reflex was 2.85 mV, and the mean amplitude of the corresponding m-wave was 0.74 mV.
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2 = 0.07). An identical pattern of results was obtained, when the amplitude of each f-wave was expressed as a ratio of the corresponding m-wave response (F1,7 < 1, P > 0.20, f = 0.27). In conditions in which the opposite limb was moving, the mean amplitude of the f-wave (averaged across participants) was 0.43 mV, and the mean amplitude of the corresponding (maximal) m-wave was 8.74 mV. In the control condition, in which the opposite limb was at rest, the mean amplitude of the f-wave was 0.76 mV, and the mean amplitude of the corresponding m-wave was 8.59 mV. Stretch reflexes
In all of the eight individuals investigated, stretch of the wrist flexors evoked two distinct bursts of reflex activity in FCR at mean onset latencies of 31 ± 5 and 45 ± 5 ms. These were termed the short latency (SL) and long latency (LL) components of the reflex. An example from one participant is illustrated in Fig. 6A. For each condition, i.e. for each phase of the movement of the opposite limb, average rectified responses (n 20) were obtained. The integrated EMG (i.e. the area under the average full-wave rectified curve) was calculated separately for the two components of the reflex on the basis of the onset and offset latencies obtained from the static control trials.
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2 = 0.31). The responses recorded during phases 4 and 5 were larger than those obtained during phases 1, 2, 3, 7 and 8 (P < 0.05). In addition, responses elicited during phase 6 were larger than those recorded during phases 1, 2 and 8 (P < 0.05). A similar pattern of variation was obtained for the LL component of the reflex response (F1,7 = 3.71, P < 0.01, f = 0.64, 2 = 0.25). In this case, the responses recorded during phases 4, 5 and 6 were larger than those elicited during phases 1, 2, 7 and 8 (P < 0.05). For both components of the reflex response, there was variation between the participants with respect to the mean magnitude of the responses upon which the phasic modulation was superimposed. As a consequence when the values were pooled, they did not differ reliably from the control responses. |
Discussion |
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Responses to TMS recorded in the muscles of the upper limb are induced primarily by the trans-synaptic excitation of corticospinal cells. While the amplitude of the MEP thus reflects the excitability of neurones in the motor cortex (Rothwell et al. 1991), it is also influenced by the state of the spinal motoneurone pool. As a consequence, it is not possible on the basis of TMS alone to determine the precise elements of the motor pathway that are responsible for the variations in response amplitude which are observed in an experimental task. Responses evoked by stimulation of the corticospinal tract at the level of the cervicomedullary junction (CMEPs) are mediated by many of the same axons activated by magnetic stimulation of the motor cortex (Gandevia et al. 1999; Taylor et al. 2002; Ugawa et al. 1991). In the present study, MEPs recorded in the quiescent right FCR were potentiated during the phases of movement of the opposite limb in which the left FCR was most active (Carson et al. 1999; Stinear & Byblow, 2002). In contrast, the CMEPs recorded from the right FCR were not influenced by movements of the opposite limb. This suggests that the excitability of the spinal motoneurone pool did not change. It is possible to infer therefore that the potentiation and modulation of the responses evoked by TMS were due to changes in the excitability of the motor cortex.
A similar pattern of outcomes was obtained recently by Hortobágyi et al. (2003), who observed that during moderate to strong isometric contractions of the left wrist flexor muscles, MEPs evoked by TMS in the right FCR were larger than those obtained at rest. In addition, the degree of crossed facilitation of the homologous motor pathway was contingent upon the level of contraction generated by the active muscle (e.g. Hess et al. 1986; Stedman et al. 1998; Muellbacher et al. 2000). Potentials evoked by stimulation of the cervicomedullary junction were, however, unaffected by contraction of the muscles of the opposite limb. These findings lend support to the conclusion that the modulation of excitability in the corticospinal pathways observed in the present study was attributable to phasic alterations in descending drive to the homologous muscle, rather than due simply to the rhythmic movement of the opposite limb. Indeed, in circumstances in which similar unilateral movements are induced passively, the MEPs recorded in the static limb are not modulated and are smaller than those obtained at rest (Carson et al. 2000).
In a recent study, Sohn et al. (2003) obtained MEPs in several muscles of the left arm during discrete self-initiated movements of individual fingers of the right hand. During the period immediately following EMG onset, there was a diffuse inhibition of responses evoked by TMS in the muscles of the opposite arm. The extent of this inhibition was lower in the homologous muscle than in other adjacent muscles. There was also a marked increase in interhemispheric facilitation in the motor cortex ipsilateral to the voluntary contractions, the expression of which was confined to the homologous muscle of the left hand. No changes in interhemispheric inhibition were observed. It thus appears that when a muscle acts as a prime mover in a specific task context, there exist excitatory relations between the cortical representation of the muscle and that of its homologue. When the muscle is not engaged as a prime mover, inhibitory interhemispheric relations prevail (Carson & Riek, 2000).
In the present study, increases in the excitability of the cortical representation of FCR were observed during rhythmic movements of the opposite limb, in which the wrist flexor (and extensor) muscles were the prime movers. The most parsimonious explanation of this interhemispheric facilitation is that the phasic descending drive directed to the muscles of the moving limb was also transmitted by collaterals of corticospinal neurones, which project via the corpus callosum, to the homotopic area of the contralateral motor cortex (Hanajima et al. 2001). The neuroanatomical evidence for such projections, however, remains sparse. It may also have been the case that the crossed facilitation had as its basis common inputs from motor centres upstream of primary motor cortex, and as its substrate the dense transcallosal projections which link secondary motor areas such as cingulate cortex. The possibility that bilateral activation in primary motor areas may first arise in the cingulate cortex of the opposite hemisphere, spread through the callosal fibres to the ipsilateral cingulate cortex and subsequently to M1 is supported by observations in neurologically healthy human subjects. In these subjects, the activity registered in cingulate cortical areas during both unimanual and bimanual movements is correlated positively with the size of the corpus callosum (Stancák et al. 2003).
It is conceivable that the crossed facilitation of MEP responses could have been mediated, at least in part, by subcortical structures or by afferent input projecting to the higher motor centres via sensory areas. There is evidence of bilateral representation of upper-limb muscles in human secondary somatosensory cortices (SII), and to a lesser extent in primary somatosensory cortex (SI) (Simões et al. 2001). In particular, somatosensory-evoked magnetic fields (SEFs) induced by peripheral nerve stimulation reveal prominent ipsilateral responses in SII (Karhu & Tesche, 1999; Simões & Hari, 1999; Wegner et al. 2000). There are, however, few indications that the responsiveness of SII neurones changes during movements of the opposite limb (Huttunen et al. 1996; Nakata et al. 2003, 2004).
In the lower limb, the amplitude of the spinal H-reflex is modulated in phase with voluntary movement of the opposite leg (McIlroy et al. 1992). It has been proposed previously that effects of this nature, if they are also present in the upper limb, may be implicated in the control and stability of bimanual coordination (Carson et al. 1996). In the present study, the H-reflexes elicited in the quiescent right FCR during rhythmic movements of the left wrist were depressed profoundly with respect to those obtained when both limbs were at rest. In addition, H-reflex amplitudes, and those of both the SL and LL components of the stretch reflex, were modulated during movement of the opposite limb. The largest reflex responses were obtained during those phases of movement in which the opposite (left) FCR was most active (Carson et al. 1999). f-waves were also evoked in right FCR, in order to assess the excitability of the spinal motoneurones. f-Waves are the late motor response to supramaximal stimulation of the peripheral nerve that arise from antidromic activation of the motoneurones. In the present study, and in contrast to the H-reflex responses, the f-wave amplitudes were not modulated during movements of the opposite limb. As CMEPs were likewise of constant amplitude, it may be concluded that the phasic modulation of the H-reflex was mediated by presynaptic inputs to the Ia afferents, rather than by postsynaptic inhibition or disfacilitation of the motoneurones.
A similar pattern of modulation may be obtained in the resting forearm during rhythmic movements of the foot. When the forearm is placed in a prone position, the FCR H-reflex increases during plantarflexion, and decreases during dorsiflexion of the foot (Baldissera et al. 2002; Cerri et al. 2003). On the basis of the observation that these variations are largely abolished when the H-reflex is elicited during the cortical silent period that follows TMS, Baldissera et al. (2002) argued that the reflex modulation is generated by corticospinal rather than by segmental inputs. Converging evidence that the systematic variations in reflex amplitude may be contingent upon descending input is provided by the observation that when movements of the opposite wrist are induced passively, there is no corresponding modulation of H-reflex amplitude (Carson et al. 2000). It has also been noted that the pattern of variation of the H-reflex evoked in FCR during movements of the foot is tied more closely to the EMG activity of the muscles that cross the ankle, than to the kinematic profile of the foot (Cerri et al. 2003). In the present experiment, it was also the case that the largest H-reflex responses were obtained during the phases of the movement in which the homologous muscle of the opposite limb was most strongly engaged. In contrast, during isometric contractions of the upper limb musculature, the size of the H-reflex evoked in the opposite limb scales in an inverse fashion with the intensity of the contraction (Hortobágyi et al. 2003).
While it appears that the phasic modulation of the H-reflex may arise from presynaptic inhibition of Ia afferents mediated by descending inputs, the origin of the overall depression of the H-reflex is less clear. Inhibition of the FCR H-reflex both during and following isometric contractions of the homologous muscle of the opposite limb has been reported by Hortobágyi et al. (2003). As there were no corresponding changes in the amplitude of CMEPs, the depression was ascribed to presynaptic mechanisms. In the present study, while we also failed to observe a diminution of responses to cervicomedullary stimulation, f-waves were depressed markedly by movement of the opposite limb. It is unlikely that the population of motoneurones activated by the Ia afferent volley giving rise to the H-reflex will have overlapped precisely with that recruited by the descending corticospinal volley evoked by stimulation of cervicomedullary junction, or with that activated by the antidromic stimulation used to elicit f-waves. It is reasonable to conclude that both stimulation of the Ia afferents (Hugon, 1973) and of the cervicomedullary junction (Taylor et al. 2002) recruits motor units in physiological order in accordance with the size principle. The potentials evoked by cervicomedullary junction stimulation in the present experiment (control amplitude 0.24 mV) are likely to have engaged motor units that were on average smaller than those which mediated the H-reflex responses (control amplitude 2.85 mV). It is also generally assumed that f-waves are elicited by the selective (antidromic) activation of the largest, fastest conducting motor units (e.g. Vatine & Gonen, 1996). It is possible, therefore, that the observed depression of the H-reflex was mediated by postsynaptic inhibition or disfacilitation of the largest units in the motoneurone pool, an effect that would also be expressed in a diminution of f-waves, but not in the responses to stimulation of the cervicomedullary junction. It has been argued previously (Aimonetti et al. 2001) that, in the context of manipulatory finger movements and gripping tasks, in which the wrist extensor and flexor muscles act as functional synergists, transmission in the reciprocal disynaptic Ia pathways may be modulated by central descending fibres which converge with sensory afferents on spinal interneurones. These mechanisms appear to afford a means of controlling independently the firing patterns of the low- and high-threshold motor units in these muscles in a task-specific fashion. To our knowledge, the possibility that similar mechanisms may mediate the crossed inhibition of high-threshold motor units has not yet been addressed.
In this regard, it is notable that while the amplitude of the H-reflex was depressed markedly during rhythmic movements of the opposite limb, neither component of the stretch reflex exhibited a corresponding effect. The stretch responses were of appreciably smaller amplitude than the H-reflexes, suggesting that somewhat different subpopulations of motor units were engaged. There are, however, other factors which may have accounted for the differences between the two responses. The H-reflex is mediated primarily via a Ia pathway, whereas it is likely that group II afferents also contribute to the stretch reflex (Kanda & Rymer, 1977). In addition, while the H-reflex is thought to be largely monosynaptic (cf. Burke et al. 1984), stretch reflexes may involve polysynaptic pathways which are subject to the influence of a variety of descending and segmental inputs (Rothwell, 1994). To the extent that these influences are altered by movement of the opposite limb, a means is provided of regulating the sensitivity of the stretch reflex response beyond that furnished by presynaptic inputs to Ia afferents. Finally, it is possible that movements of the opposite limb give rise to alterations in gamma drive, thus changing the sensitivity of the muscle spindles. Any such effects would be reflected in the stretch reflex, but not in the H-reflex response.
There was some indication that the SL component of the stretch reflex (31% of the variance attributable to movement phase) may have been modulated to a greater degree than the LL component (25% of the variance attributable to movement phase). It has been proposed that Ia inputs contribute to a larger degree to the SL component of the stretch reflex response than to the LL component, as the latter may also be mediated in part by inputs from skin and subcutaneous receptors (Corden et al. 2000). If the modulation of the stretch reflex that arises during movement of the opposite limb is mediated primarily by presynaptic inputs to Ia afferents, a more prominent expression of this effect in the SL component would therefore be anticipated. There are also strong indications that the LL component of the stretch response in FCR is mediated, at least in part, by a transcortical pathway (Lewis et al. 2004), and may submit to independent control. The SL and LL components of upper limb stretch reflexes may also be conditioned separately (Segal et al. 2000). Taken together, these results suggest that an uncoupling of the two components may occur in specific task contexts.
It is clear that bimanual coordination does not arise simply from the superposition of two unimanual movements. There are principles governing bimanual coordination which cannot be inferred from the control of single limb movements. Nonetheless, it is essential to determine those features of observed behaviour which can be accounted for on the basis of bilateral interactions arising from unimanual movements, before invoking mechanisms that are specific to bimanual coordination. The results obtained in the present study provide no evidence to support the view uncrossed corticofugal fibres or branched bilateral corticomotoneuronal projections mediate excitatory interactions between the limbs. While the potentials evoked by TMS were potentiated in a phasic fashion during rhythmic movements of the opposite limb, there were no corresponding changes the excitability of the spinal motoneurones. Indeed, the observed depression of the f-wave responses suggests that rhythmic movements of the opposite limb may give rise to disfacilitation of the largest units in the spinal motoneurone pool. Our findings indicate that, during movements intended to be unilateral, interhemispheric interactions between cortical motor areas modulate the excitability in motor pathways projecting to the homologous muscles of the opposite limb. These interactions are likely to favour patterns of rhythmic coordination in which homologous muscles are engaged simultaneously, and to disrupt those in which homologous muscles are activated in an alternating fashion. Rhythmic movements of the opposite limb also modulate, via (presynaptic) inhibition of Ia afferents (e.g. Hortobágyi et al. 2003), segmental inputs to spinal motoneurones. It remains to be resolved whether these segmental effects play a functional role with respect to the stability of inter-limb coordination.
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References |
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Baldissera F, Borroni P, Cavallari P & Cerri G (2002). Excitability changes in human corticospinal projections to forearm muscles during voluntary movement of ipsilateral foot. J Physiol 539, 903–911.
Burke D, Gandevia SC & McKeon B (1984). Monosynaptic and oligosynaptic contributions to human ankle jerk and H-reflex. J Neurophysiol 52, 435–448.
Carson RG, Byblow WD, Abernethy B & Summers JJ (1996). The contribution of inherent and incidental constraints to intentional switching between patterns of bimanual coordination. Hum Mov Sci 15, 565–589.[CrossRef]
Carson RG, Byblow WD, Riek S, Lewis GN & Stinear JW (2000). Passive movement alters the transmission of corticospinal input to upper limb motoneurones. In Abstracts for 30th Meeting of Society for Neuroscience, pp. 1231. New Orleans, USA.
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