Prime mover muscle in finger lift or finger flexion reaction times: identification with transcranial magnetic stimulation

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Electroencephalography and clinical Neurophysiology , 81 (1991)319-322 © 1991 Elsevier Scientific Publishers Ireland, Ltd. 0924-980X/91/$03,50 A D O N I S 0924980X9100090K

E L M O C O 91547

Short c o m m u n i c a t i o n

Prime mover muscle in finger lift or finger flexion reaction times: identification with transcranial magnetic stimulation Claude Tomberg

a

and Maria D. Caramia b

a Brain Research Unit, Unit,ersity o f Brussels, Brussels (Belgium), and b Department of Neurology, Tor Vergata University, Rome (Italy) (Accepted for publication: 4 April 1991)

Summary

W h e n recording the onset of the electromyographic ( E M G ) voluntary response in reaction time (RT) studies, the electrodes should be placed on the muscle which is first and foremost involved in executing the response. It is thus necessary to identify which is the prime mover muscle a m o n g active synergic muscles. This has been investigated for index finger lift or flexion R T s by delivering a magnetic stimulus to motor cortical areas prior to the subject's voluntary response. T h e E M G responses to the magnetic stimulus were selectively facilitated either in the extensor indicis proprius muscle (in index lift RTs) or in the first dorsal interosseous muscle (in index flexion RTs). These effects are robust and provide a method for identifying the prime mover muscle in voluntary movements.

Key words: Magnetic motor stimulation; Reaction time; Electromyography; Prime mover muscle; Nerve stimulation

Studies of reaction times (RTs) frequently include the electromyographic ( E M G ) recording of the muscles executing the subject's motor responses, such as in finger lift or finger flexion R T s (Tomberg et al. 1991). Index finger lift can involve the extensor indicis proprius and extensor digitorum communis muscles, while index finger flexion can be achieved by the first dorsal interosseous and the flexor digitorum communis muscles. For E M G onset to be consistently recorded in each case, the E M G electrodes should be placed over the muscle which is first and foremost involved in the R T response. The problem of identifying the prime mover muscle has been tackled by using transcranial magnetic stimulation (TMS) of cortical motor areas (Barker et al. 1985) and recording the E M G response of the muscles that move the index finger. It is well known that responses to T M S present a latency shortening of 2 - 6 msec and an enhanced voltage when the target muscle is steadily contracted (Hess et al. 1987; Rossini and Caramia 1988). A similar facilitation has also been recorded in relaxed muscles during the 80 msec that precede a transient voluntary contraction of the target muscle (Rossini and Caramia 1988; Rossini et al. 1988; Starr et al. 1988). In the present study, subthreshold TMS evoked E M G responses that were selectively facilitated either in the extensor indicis proprius muscle (in index lift RTs) or in the first dorsal interosseous muscle (in index flexion RTs). Such selective TMS effects provide a new method for identifying the prime mover muscle in voluntary movements.

Methods Five healthy adults (25-39 years) gave informed consent for experiments using a magnetic circular coil of 7 cm internal diameter

Correspondence to: Dr. Claude Tomberg, Brain Research Unit, 20 rue Evers, Brussels 1000 (Belgium). Tel.: 322-536.61.89; Fax: 322-536.61.94.

(CadweU MES-10) placed on the left central scalp. T h e intensity of the brief magnetic pulse was expressed as a percentage of maximal output (2.5 tesla) and was kept constant during any run. The magnetic coil was carefully maintained in the same position over the head throughout the run to ensure stability of the stimulus. Surface E M G s (belly tendon) were recorded with Medelec stick-on electrodes over the motor endplate zone (Desmedt 1958; T o m b e r g et al. 1991) of the right extensor indicis proprius and extensor digitorum communis muscles for index extension R T s (Fig. 1A) or over the right first dorsal interosseous and flexor digitorum communis muscles for index flexion RTs (Fig. 1B). The R T signal was a brief electric pulse delivered at random intervals of 5 - 1 0 sec to the left t h u m b (intensity 2 - 3 times the subjective threshold). T h e magnetic stimulus was triggered 90 msec after the R T signal. Before each trial of a run, the subject was verbally instructed (according to a r a n d o m sequence) to either ignore the R T signal, or to respond rapidly to it by a slight extension (lift) or flexion of the right index while keeping muscles otherwise relaxed.

Results

Peripheral nerve stimulation Latencies to nerve stimulation were m e a s u r e d in preliminary experiments. For a single maximal shock on the radial nerve, about 10 cm above the elbow on the external side of the arm, the onset latencies of the belly-tendon E M G were on average 1.5 msec longer for the extensor indicis proprius than for the extensor digitorum c o m m u n i s (Fig. 1A) the motor point of which is located about 9 cm more proximally (Tomberg et al. 1991). T h e belly-tendon responses of the first dorsal interosseous (ulnar nerve) and flexor digitorum c o m m u n i s (median nerve) were compared for stimulation of these nerves 4 cm above the elbow (Fig. 1B). T h e latencies were about 4 msec longer for the interosseous. The data corresponded to a maximal conduction velocity of about 60 m / s e c in the forearm s e g m e n t of these motor nerves (cf., Trojaborg and Sindrup 1969; Kimura 1983).

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Suprathreshold TMS We also tested TMS intensities slightly above threshold which elicited E M G responses of about 0.1 mV in both flexor muscles. The E M G responses were similar when the subject was told to ignore the R T signal (Fig. 4A). The latencies were 22.1 msec in the (relaxed) first dorsal interosseous (FDI) and 19.2 msec in flexor digitorum communis (FDC). Such latency difference of about 3 msec obviously reflected the extra conduction distance from the brain for FDI. In trials when the subject made a slight voluntary response to the R T signal, the FDI response to TMS was significantly enhanced while the F D C response was either markedly reduced or suppressed

Subthreshold transcranial magnetic stimulation (TMS) The threshold TMS intensity for eliciting a muscle response was first defined by the m e t h o d of limits in the relaxed subject. In the subsequent experimental runs, the T M S intensity was fixed at about 10% below this threshold value. We found that no E M G response was evoked by TMS in all the trials for which the subject was told to ignore the R T signal (Figs. 2A and 3A). In the randomly intermixed trials for which the subject was told to respond by a brief index lift, the extensor indicis proprius showed a sizable E M G response to TMS with a latency of about 18.5 msec and this was followed by the R T voluntary response about 55 msec later (Fig. 2B). The simultaneously recorded extensor digitorum communis consistently showed much smaller E M G responses of similar latencies. In other runs, the subject had to make a slight index flexion as R T response. T h e first dorsal interosseous (FDI) was then usually the only index flexor showing an E M G response to the subthreshold TMS (Fig. 3B). There were no E M G responses in the trials for which the subject was told to ignore the R T signal (Fig. 3A). In a few trials, the subject happened to respond with a stronger R T voluntary flexion and the E M G response to TMS was markedly enhanced in FDI but only slightly in the flexor digitorum c o m m u n i s muscle (FDC; Fig. 3C). The latency of the F D C response to T M S was not shorter and sometimes actually slightly longer than the latency of FDI. Obviously, the stronge-r facilitation of the interosseous response to subthreshold T M S involved a substantial latency shortening whereby

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(Fig. 4B). This consistent finding suggests that, during the preparation of R T response, the prime mover was facilitated while the synergic flexor muscle was actually inhibited. In the trials when the subject made a stronger R T response, the E M G response to TMS was facilitated in both FDI and FDC.

O n this basis, we consider the facilitatory effects to be phasic and to be transiently elicited in the motor cortical areas during each trial, precisely at the point in time when the R T signal has received sufficient perceptual processing (see D e s m e d t and T o m b e r g 1989) to warrant the release of an 'intention to move' the target muscle. It has been suggested that the facilitatory effect of steady voluntary contraction on the E M G response to TMS would primarily involve spinal mechanisms at the level of motoneurons (Maertens de Noordhout et al. 1989; Rothwell et al. 1989). These considerations should not be extrapolated to the rather different situation of our study in which the TMS facilitation is recorded in a fully relaxed muscle. We think that, under such conditions, the facilitatory effects must be intermittently released in register with the kinetics of cognitive brain mechanisms. It must indeed be emphasized that TMS facilitatory effects can be remarkably selective a m o n g spinal motoneurons when the intended voluntary movement is skilled and precisely targeted to achieve a well-defined movement (here a slight index lift or flexion)• Our results indicate that the physiological preparation differentially involves the motor pyramidal pathways to the muscle which will actually be the first and foremost to execute the selected movement (Figs. 2 and 3). They also reveal that the cortical motor areas related to other synergic muscles may actually be concurrently inhibited (Fig. 4) if the voluntary movement is indeed precisely targeted. The method based on TMS testing during the preparation to execute a voluntary response appears to be remarkably suited for identifying the prime mover muscle among all the muscles which can be involved in a given voluntary performance. We wish to thank Paolo Rossini (Rome) and John E. Desmedt (Brussels) for their valuable support and advice. This research has been supported in part by grants from the Fonds de la Recherche Scientifique M~dicale, Belgium and from the Consiglio Nazionale delle Ricerche, Italy•

References Discussion

Contraction of target muscles is known to enhance the voltage and reduce the latency of E M G responses to transcranial electric (Merton and Morton 1980; Rothwell et al. 1987, 1989) or magnetic (Hess et al. 1987; Rossini and Caramia 1988) stimulations. T h e latency effect was said to be smaller in the case of magnetic stimulation (Rothwell et al. 1989). However, we found that the excess peripheral conduction time for the interosseous as compared to the flexor digitorum communis (Fig. 1B) could be more than compensated through differential facilitation of the interosseous response to magnetic stimulation (Fig. 3C). Previous studies demonstrated facilitatory effects in relaxed muscles during the 80 msec that precede a transient voluntary contraction of the target muscle (Rossini and Caramia 1988; Rossini et al. 1988; Starr et al. 1988). In many studies the facilitation was rather diffuse a m o n g limb muscles, but precise assessment of its actual extent in limb muscles can be compromised by failure of the subject to completely relax during the tests (Hess et al. 1987). We found that subthreshold TMS evoked E M G responses that were selectively facilitated either in the extensor indicis proprius muscle (in index extension RTs) or in the first dorsal interosseous muscle (in index flexion RTs). T h e facilitatory effect was absent in intermixed 'catch' trials in which the subject indeed received the same R T signal but was told to just ignore it. The lack of E M G response to subthreshold T M S in such 'ignore' trials showed that the facilitation could not be ascribed to any general motor set that would have prevailed throughout the experimental run.

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