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Excitability of the H-reflex in the relaxed flexor carpi radialis (FCR) muscle was tested during voluntary oscillations of the ipsilateral foot at five evenly spaced delays during a 600 ms cycle. In some experiments the H-reflex was conditioned by transcranial magnetic stimulation (TMS). With the hand prone, the amplitude of the FCR H-reflex was modulated sinusoidally with the same period as the foot oscillation, the modulation peak occurring in coincidence with contraction of the foot plantar-flexor soleus and the trough during contraction of the extensor tibialis anterior. When the H-reflex was facilitated by TMS at short latency (conditioning-test interval: −2 to −3.5 ms), the modulation was larger than that occurring with an unconditioned reflex of comparable size. This suggests that both the peripheral and the corticospinal components of the facilitated response were modulated in parallel. When the H-reflex was tested 40–60 ms after conditioning, i.e. during the cortical ‘silent period’ induced by TMS, no direct effect was produced on the reflex size but the foot-associated modulation was deeply depressed. These results suggest that the reflex modulation may depend on activity fluctuations in the cortical motor area innervating the forearm motoneurones. It is proposed that when the foot is rhythmically oscillated, along with the full activation of the foot cortical area a simultaneous lesser co-activation of the forearm area produces a subliminal cyclic modulation of cervical motoneurones excitability. Should the two limbs be moved together, the time course of this modulation would favour isodirectional movements of the prone hand and foot, indeed the preferential coupling observed when hand and foot are voluntarily oscillated.
In this context, the term nervous constraint usually refers to factors, or situations, which limit the coupling repertoire, such as for instance those factors hindering or impeding non-isodirectional coupling of ipsilateral limbs. The term constraint, however, may be understood not as a limit but rather as an obligation to produce a certain behaviour. In this view, the existence of a clear-cut preference for isodirectional (in-phase) coupling of ipsilateral limbs may be regarded as the expression of a nervous arrangement that binds the limbs to ‘imitate’ each other whenever they are moved simultaneously. This same nervous arrangement would discourage other types of coupling, for instance in phase opposition.
Along these lines, it was recently reported that during the voluntary rhythmic flexion-extension movement of the foot the H-reflex excitability in the resting forearm undergoes cyclic modulation (Baldissera et al. 1998). With the forearm in prone position, the phase of increased excitability in the flexor carpi radialis (FCR) muscle coincided with the foot plantar flexion. To account for these findings, it might be postulated that afferent signals generated by the foot movement influence the reflex excitability in the cervical spinal segments. However, it was also recently demonstrated that the cyclic modulation of the H-reflex in the resting forearm is not related to movement, but temporally bound to the activation of foot movers (Baldissera et al. 2001). This makes a kinaesthetic origin of the modulation unlikely and points to a central origin. In this light, one could envision that when the foot is moved in isolation, central motor areas send supraliminal commands to the foot and subliminal collateral influences in the motor pathways directed to the non-moving hand. If this hypothesis, which proposes a neural substrate for the isodirectional coupling of hand and foot, is correct, it should be possible to monitor excitability changes in the cortical motor areas projecting to the resting hand during voluntary movement of the foot.
On this basis, we explored the excitability of the corticospinal projection to FCR muscle during cyclic flexion-extensions of the ipsilateral foot, combining transcranial magnetic stimulation (TMS) with H-reflex testing.
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The reported cyclic excitability changes in H-reflex, occurring in a resting forearm muscle during voluntary oscillation of the foot, may depend either on cyclic changes of motoneurone membrane potential or on modulation of presynaptic Ia terminals. At this stage we were not directly interested in the spinal mechanism responsible for the modulation and did not try any more direct investigation on presynaptic inhibition. However, some inferences concerning this problem may be derived from the following observations. If the modulation were exclusively operated by means of primary afferent depolarisation (PAD) in Ia terminals, then the facilitated H-reflex, which results from the sum of the descending and afferent-components, should be less influenced than the pure H-response, which is exclusively due to Ia EPSPs. The present data, instead, show that the TMS-facilitated H-reflex undergoes a deeper modulation than the unconditioned response. In addition, the CMAPs directly evoked by TMS underwent a clear-cut modulation (parallel to that of the H-reflex), despite the fact that changes in PAD of Ia terminals should not influence the corticospinal EPSPs. Thus, since the presynaptic terminals of cortico-motoneuronal fibres do not apparently undergo presynaptic inhibition (Nielsen & Petersen, 1994; Rudomin & Schmidt, 1999), it should follow that during foot voluntary movements motoneurone excitability is indeed modulated post-synaptically. It is worth mentioning, however, that postsynaptic effects may be induced in motoneurones if a steady afferent inflow to them is modulated by cyclic variations of PAD.
A more urgent question, from our present perspective, concerns the origin of the modulation, in particular whether it is a feedback action, generated by the kinaesthetic afferences from the foot movements, or a central action directed in parallel both to the moving lower limb and, with subthreshold intensity, to the neurones innervating the resting upper limb.
The aim of the present experiments was to explore whether the corticospinal neurones projecting to the forearm muscles undergo excitability changes parallel to those occurring at the spinal level during foot oscillations. In this regard, the corticospinal excitability was probed by TMS conditioning of the H-reflex at two conditioning-test intervals. Short-interval conditioning, which induces facilitation of the H-response, demonstrated a combined increase in both the motoneuronal reflex excitability and the descending action, the latter suggesting a cyclic variation in the excitability of corticospinal neurones. Admittedly, a modulation of the corticospinal effect might also result from segmental facilitation of propriospinal neurones, which are presumed to mediate disynaptic EPSPs from the corticospinal tract to motoneurones (Burke et al. 1994; Gracies et al. 1994). This possibility, however, should be ruled out, since we tested the H-reflex facilitation at intervals at which only the monosynaptic cortico-motoneuronal excitation is acting. Thus, the increased corticospinal effects indeed appear to depend on changes in cortical excitability. In turn, at long conditioning-test intervals (‘silent period’) TMS evoked a cortical depression that effectively reduced the H-reflex modulation, but it did not produce substantial effects on the H-reflex itself. Such a finding strongly suggests that the motoneuronal excitability changes associated with foot oscillations were produced by a corticospinal influence, since they disappeared during the periods of post-stimulus cortical inhibition. Thus, beyond confirming the occurrence of excitability changes in the hand motor area during cyclic voluntary movements of the foot, this added evidence favours the idea that the H-reflex modulation is actually induced by descending activities from the motor cortex.
A few considerations seem worthwhile regarding the cortical depression associated with the ‘silent period’. Most studies (Davey et al. 1994; Classen & Benecke, 1995; Mills, 1999) agree that the silent period after TMS is mainly a cortical phenomenon; nevertheless, we kept TMS intensity subliminal for motor responses (but sufficient to excite corticospinal neurones, as witnessed by the short-latency facilitation of the H-reflex) in order to avoid any interference due to peripheral post-spiking refractoriness. At this intensity TMS still evokes suppression of voluntary EMG (Davey et al. 1994). Recent results suggest that the inhibitory phenomena during the silent period not only affect the corticospinal neurones but also suppress the motor drive to them (Tergau et al. 1999). This would fit well with the working hypothesis inspiring this investigation, i.e. that when the foot is rhythmically oscillated the hand cortical area is co-activated, producing a modulation of its descending output to cervical motoneurones. Suppression of the co-activation drive during the silent period may thus contribute to the flattening of the motoneuronal excitability modulation. In this regard, it is also worth mentioning that the existence of strong functional interactions between the foot and hand areas of the motor cortex during coupled movements of the two limbs is suggested by the recent finding (Liepert et al. 1999) that the output map for the thumb movers shifts apart during and after coupled synchronous movements of the thumb and ipsilateral foot. In light of this, the present results, showing the occurrence of excitability changes in the hand area when only the foot is moved, could be taken as evidence that such interactions, though weakened, are also present when one limb is moved in isolation. Further support to the hypothesis that the spinal motor structures innervating hand and foot are activated in parallel also comes from the recent observation that the cyclic modulation of the H-reflex in the resting forearm is temporally bound to the muscular activation of foot movers, not to movement (Baldissera et al. 2001).
Altogether, this evidence leads us to propose that, during oscillations of the foot, parallel excitability changes occur in both foot and hand cortical areas. Conversely, this same evidence suggests that the H-reflex modulation should not be caused directly by kinaesthetic signals from the movement of the foot. An afferent origin of the cortical modulation cannot, however, be ruled out. It might in fact be hypothesised that afferent signals generated by cyclic muscle contraction (not by movement) may reach the hand cortical area and periodically affect its excitability.
With regard to the functional implications, these results should first be discussed in the context of the co-ordination of coupled limb movements. As already suggested, the time course of the FCR excitability changes would favour isodirectional coupling when the hand and foot are oscillated together. It is open to question, however, whether the relatively small effect disclosed by our experiments is sufficient to determine the well-assessed preferential coupling between isodirectional hand and foot oscillations. In this regard, two aspects should be recalled. First, the strong interaction between the hand and foot cortical areas observed when both limbs move together (Liepert et al. 1999) is in keeping with the idea that, during coupling, the influences that bind the two areas may increase sufficiently to sustain the isodirectional preference. Second, it should also be remembered that the coupling between hand and foot during in-phase oscillations is rather loose, as witnessed by the possibility of voluntarily performing anti-phase oscillations as well as by the compensatory reaction that occurs after inertial loading of one segment (Baldissera & Cavallari, 2001), which mainly consists of anticipating the activation of the muscles that move the loaded segment.
It might finally be argued that preferential coupling of isodirectional movements of the hand and foot has hardly any obvious purpose in ordinary behaviour. This is probably the reason why such a coupling is usually described as a constraint, rather than as an organisation pattern, as happens, for example, for the various types of limb coupling related to locomotion (cf. Orlovsky et al. 1999). An economy principle would predict that any motor organisation should not have developed without some functional pressure. Thus it seems interesting to speculate how to categorise hand-foot coupling within the context of motor control. In this regard, the ‘anticipatory postural activities’ (APAs; Marsden et al. 1978; Marsden et al. 1981; Cordo & Nashner, 1982; Bouisset & Zattara, 1987; Zattara & Bouisset, 1988) show appealing similarities to the co-activation described here. For instance, they are characterised by the parallel activation of muscles in different body segments, they are scaled with the intensity of the prime movement (Aruin & Latash, 1996) and can be reduced or abolished when the biomechanical context is modified (Aruin et al. 1998). Their scope is either to prepare a fixation chain connecting the moving segment to a firm support, or to produce a motor action that contrasts the postural unbalance produced by the main body action. It is of interest that when performing wrist flexion-extension while trying to maintain a constant limb posture, APAs develop in the upper limb which are characterised by directional postural synergies (Chabran et al. 1999). Moreover, it has been repeatedly demonstrated that both the timing and the spatial distribution of the APAs may vary when the surround conditions or some feature of the movement (e.g. direction) are changed (Nashner & Forssberg, 1986; Aruin & Latash, 1995). This allows us to postulate that even when a manifest intervention of the APA is not required, as in our experimental condition (a sitting subject with the foot supported by the oscillating platform), subthreshold effects may nevertheless take place. According to this view, the positive and negative constraints characterising ipsilateral limb coupling might indeed be an expression of some underlying postural mechanism.