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INTEGRATIVE |
1 Department of Neurology, Charité, Humboldt University of Berlin, 10117 Berlin, Germany
2 Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square, London, UK
3 Department of Psychiatry, Charité University Hospital/St Hedwig Hospital, 10559 Berlin, Germany
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Abstract |
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(Received 28 February 2005;
accepted after revision 30 March 2006;
first published online 31 March 2006)
Corresponding author J. C. Rothwell: Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London, London WC1N 3BG, UK. Email: j.rothwell{at}ion.ucl.ac.uk
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Introduction |
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In the past there has been some debate over the origin of the EMG pattern. The equilibrium point hypothesis (see for instance Feldman et al. 1995; Feldman & Latash, 2005) postulates that the CNS initiates a movement by changing the activation threshold of motoneurones. In this model, length- and velocity-sensitive reflexes are the predominant mechanisms for generating EMG patterns. However, although reflexes may modulate the EMG bursts, there is now considerable evidence that the majority of the triphasic pattern is generated centrally (Gottlieb, 1998a,b, 2001). For example, Gottlieb et al. (1989) demonstrated that EMG, torque and kinematic patterns depend on parameters of the movement task and that the earliest differences in EMG pattern occur before differences in kinematics. Thus these cannot be due to reflex events set up by the movement itself. Similarly, the triphasic EMG bursts are present in deafferented patients (Forget & Lamarre, 1987), although they are not timed as accurately relative to the parameters of movement as in subjects with intact sensation, suggesting that afferent feedback is needed to fine-tune the motor output (e.g. Ghez & Martin, 1982). A prominent role for central mechanisms is also consistent with the fact that in healthy subjects, the pattern of EMG bursts depends on movement strategy (Waters & Strick, 1981; Brown & Cooke, 1981); for example, the ANT is absent if subjects do not have to terminate the movement themselves. Several other observations are consistent with a relatively weak contribution from reflex mechanisms: (i) the second agonist is preserved after blockade of the motor nerve for the antagonist muscle (Garland et al. 1972), (ii) the antagonist burst is almost unchanged when the forearm is passively extended during a rapid flexion movement (Hallett et al. 1975), and (iii) the antagonist activity is no longer present if a limb is moved passively over a similar distance and velocity (Mustard & Lee, 1987).
Gottlieb (1998a) has concluded that the triphasic pattern depends on an internal model of task dynamics constructed from prior experience. This employs reflex action partially to compensate for errors or for unexpected perturbations during movement. Furthermore, it could be used for correction and updating of the internal model. Finally, volitional set may control the degree and manner in which different reflex mechanisms can contribute to the muscle activation patterns.
The present experiments were designed to investigate further the origin of the three EMG bursts. Although there is good evidence for a strong pre-programmed central input to the triphasic pattern, we know little about the detail of how this is organized. Recordings of single unit activity in monkey motor cortex show that the AG1 burst is preceded by increased neural activity (Evarts, 1966; Conrad et al. 1977) but there are no data about the relation of cortical discharge to the later components of the EMG pattern. Experiments in humans are compatible with an important role of the primary motor cortex. Day et al. (1989) found that single TMS pulses to the contralateral motor cortex delay the onset of a reaction time movement if applied in the time interval between the imperative signal and the voluntary response. Moreover, the form of the triphasic pattern is preserved, suggesting that disruption of motor cortical function delays release of the entire programme for movement, rather than interrupting just a portion. Day et al. (1989) also showed that a TMS pulse applied after onset of the AG1 could delay the ANT and AG2 suggesting that the timing of all three (and not just the AG1) of the triphasic bursts was under cortical control. Although the results from stimulation of contralateral motor cortex are clear in broad terms, they are difficult to interpret in detail because the TMS pulse evokes an MEP in the target muscles in addition to the delay in movement. The MEP changes the excitability of spinal motoneurones and also generates afferent feedback via the muscle twitch, both of which can potentially interact with subsequent voluntary motor commands related to the ballistic movement.
In order to circumvent these problems in the present study we have applied TMS pulses to the motor cortex ipsilateral to the intended movement to produce interhemispheric inhibition of corticospinal output from the non-stimulated motor cortex (Ferbert et al. 1992). Interhemispheric inhibition is best seen in subjects who are tonically contracting the ipsilateral hand muscles as a silent period in the ongoing EMG (Ferbert et al. 1992; Meyer & Röricht, 1996; Meyer et al. 1998) or as a delay in the execution of ipsilateral finger movements (Meyer & Voss, 2000) that starts about 30 ms after the pulse and lasts for approximately 30 ms. Since it is present in patients with subcortical lesions of the pyramidal system (Boroojerdi et al. 1996), and absent in patients with callosotomy or agenesis of the callosum, it is probably due to activity in a transcallosal connection (Meyer et al. 1998). This is consistent with several other sets of data: (i) H-reflexes in the relaxed forearm muscle are unaffected by conditioning stimuli of the ipsilateral hemisphere (Ferbert et al. 1992); (ii) direct recordings of descending motor volleys evoked by TMS pulses show that they are reduced in amplitude after conditioning TMS pulses to the contralateral motor area (Di Lazzaro et al. 1999); (iii) Kuhn et al. (2004) found that direct stimulation of subcortical fibres in patients with implanted electrodes for deep brain stimulation produced no ipsilateral inhibition even though the latter was clearly seen in these patients after transcranial magnetic stimulation. One study (Gerloff et al. 1998) demonstrated ipsilateral inhibition after stimulation of descending motor pathways at the level of the foramen magnum but this could have been due to activation of non-corticospinal fibres.
Given that the transcallosal inhibition operates at the level of the motor cortex, we used carefully timed short periods of cortical inhibition to probe the organization of cortical input to the ballistic movement EMG pattern. The previous results of Day et al. (1989) revealed that direct disruption of the motor cortex just before the start of each of the EMG bursts delayed the onset of that burst without changing the overall form and time relationships of subsequent bursts. This is compatible with a model in which later bursts are timed with respect to the output that generates the earlier burst. Here we ask at what time during a burst the next burst is initiated.
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Methods |
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Nine healthy volunteers (one female; age range 25–43 years) participated in the study after giving informed consent. Experiments were approved by ethics committee and were performed in accordance with the Declaration of Helsinki.
Relaxed subjects sat with their arms slightly abducted at the shoulder (about 10–20 deg) and their right elbow at an angle of about 90 deg. Their semi-pronated forearm rested on a lightweight manipulandum (construction: R. Bedlington, HMBU, National Hospital for Neurology, Queen Square, London, UK). The hand was encased in a cuff with the finger extended and the centre of rotation of the wrist joint pivoted so as to be coaxial with the axis of rotation of a shaft connected to a potentiometer.
A simple auditory reaction time protocol was used to investigate the effect of single transcranial magnetic stimulation of the primary motor cortex, given at different tone stimulus intervals (TSIs), on ipsilateral rapid voluntary movement.
Subjects were requested to perform an isotonic wrist flexion movement of about 30 deg as fast as possible. Visual feedback of the target position and actual joint position was displayed on an oscilloscope screen. The markers were clearly visible (2.1 deg x 0.9 deg of visual angle). Movements were initiated by an auditory ‘go’ tone presented randomly every 5–15 s. Subjects were trained for about 50 trials to ensure that movements were fast, and accompanied by a triphasic pattern.
Then, in 50% of the following 300–1300 trials (individually separated by pauses into blocks of 50–100 trials to avoid fatigue), single stimuli of TMS were delivered on the right motor cortex randomly between 60 and 250 ms after the onset of the auditory tone; the trials without stimulation were used as controls.
Transcranial magnetic stimulation was performed at the optimal scalp position for eliciting maximal responses in the contralateral flexor carpi radialis and extensor carpi radialis longus muscles with a stimulus intensity of 180% of the resting motor threshold using a figure-of-eight-shaped coil (90 mm outer diameter for one half coil, Magstim 200, Magstim Company, Whitland, Dyfed, UK). Coil currents were directed antero-posteriorly.
Recording
Joint position, joint velocity (electronically derived from the joint position signal), and bipolar EMG activity were recorded for each wrist movement with a 12 bit analog-to-digital converter (CED 1401, Cambridge Electronic Design, Cambridge, UK) at a sampling rate of 2 kHz per channel. EMG activity was recorded from flexor carpi radialis (FCR) and extensor carpi radialis longus (ECRL), using Ag–AgCl electrodes taped 3–4 cm apart over the muscles. EMG signals were amplified (gain 500–1000) and bandpass filtered (between 53 Hz and 1 kHz). Data were collected from the time of the auditory stimulus to 1000 ms after the tone.
Data analysis
Each single trial was inspected and analysed (see Fig. 1). Full-wave-rectified EMG signals were analysed offline by visually inspecting each single trial. Burst onset was defined as the point where EMG activity exceeded abruptly the baseline noise level. Burst offset was defined as the point where EMG activity reached baseline levels again. In most single trials onset and offset could be clearly determined. Trials with large amounts of co-contraction were excluded from analysis.
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As a control, the analysis of EMG and movement parameters was repeated in one subject using a threshold-based method. Here, onset and offset of bursts and of movement parameters were determined when activity exceeded a threshold of 10% of the maximal amplitude. In this subject, the same relative changes in the EMG pattern were noted. In three subjects, the integrated EMG activity (area under the curve) of the three EMG bursts was measured. Means and standard deviations were calculated.
The inter-onset-latencies between AG1 and ANT, as well as ANT and AG2, and AG1 and AG2 were then aligned to the time when the magnetic stimulus occurred relative to the AG1 onset and duration (see Fig. 1). The trials were grouped into the following seven different blocks according to the onset and offset of the ipsilateral silent period relative to the expected mean timing of the EMG bursts. On average the silent period starts 30 ms after TMS and lasts until 60 ms after TMS: the mean timings of the EMG bursts are given in the tables.
Effects of ipsilateral TMS could be seen and analysed in single trials. Therefore, the number of analysed trials per condition in principle should not influence the results. We analysed those single trials in which EMG burst onset and duration could be clearly determined. The number of analysed trials differed between subjects. The timing of TMS relative to movement onset lead in some subjects to the fact that only a few trials per condition could be obtained, especially for the condition 6. In those cases, values of subjects were included in the analysis if at least 10 trials per condition could be analysed. The total number of trials per condition were: control conditions, 756 trials; block 1, 264 trials; block 2a, 184 trials; block 2b, 153 trials; block 3, 75 trials; block 4, 131 trials; block 5, 146 trials; and block 6, 50 trials.
The parameters of the triphasic EMG pattern as well as movement parameters for the trials in which a cortical stimulus was applied were compared with those obtained in the control trials (see Tables 1 and 2) using a Wilcoxon signed rank test for intra-individual comparison.
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Results |
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Movements were accompanied by a characteristic triphasic pattern of EMG activity (see Fig. 1). The average onset of the AG1 burst following the auditory ‘go’ tone was 135 ± 14.5 ms (mean ± 1 S.D.), the average AG1 burst duration was 73 ± 6 ms.
Activity in the antagonist muscle consisted of an initial low level contraction that accompanied the AG1 burst, followed by a distinct increase in motor unit activity which we defined as the principal ANT burst. The initial antagonist activity began on average 12 ± 6 ms after the onset of the AG1 burst, whereas the main ANT burst began at 72 ± 7.9 ms with a duration of 73 ± 12.5 ms. The AG2 burst commenced 71 ± 11.7 ms after the ANT burst and had a duration of 58 ± 7 ms.
To further investigate the coupling between the three bursts, we measured the time between the end of AG1 and onset of ANT, and between the end of ANT and the onset of AG2. The ANT burst started 1.2 ± 7.9 ms before the end of AG1; the AG2 started 1.6 ± 6.5 ms before the end of the ANT burst.
In three subjects we obtained the integrated EMG activity (area under the curve) for each of the bursts as follows: AG1, 11 ± 2.0 mV.s; ANT, 9 ± 1.7 mV.s; area AG2, 4 ± 0.9 mV.s.
The movement lasted for 114 ± 16.3 ms, had an amplitude of 29 ± 25 deg, an acceleration duration of 70 ± 8.3 ms, and a deceleration duration of 50 ± 8.2 ms. The ratio of acceleration/deceleration was 1.4 ± 0.1.
Influence of ipsilateral TMS
Changes in distribution of reaction time induced by ipsilateral TMS. The distribution of the onset of all the three EMG bursts was changed by TMS of the ipsilateral hand motor cortex. This is illustrated in Fig. 2 in which the results as derived from the total number of trials across one subject obtained under control conditions and with TMS using a TSI of 170 ms are displayed in the form of histograms. Trials in which the TMS pulse was given have a gap of about 30 ms in the distribution of reaction times (i.e. the onset of AG1: filled arrow). Effectively, movements that in control trials began in this period are delayed until the time at which the ipsilateral silent period ends. The onset of the AG1 burst is of course unaffected by TMS pulses that occur after movement onset. However, in this case, the onset of ANT is delayed, resulting in a gap in the distribution of ANT onsets at a similar timing (filled arrow). There is also a second gap in the distribution of ANT onset (open arrow). This is the consequence of the movements in which the TMS pulse delayed AG1 onset: because the timing of all the bursts is coupled, delay in the onset of AG1 causes a delay in the onset of ANT and AG2.
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Discussion |
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Contribution of the motor cortex to the triphasic EMG bursts
There is a good deal of evidence that the AG1 burst involves activity in corticospinal projections (see Introduction), but the role of the motor cortex in the subsequent bursts is questionable. Indeed, some data from animal studies suggests that if a motor cortical unit fires in association with a muscle that contracts during AG1, it may not fire at all if the same muscle is active during the ANT burst (Flament & Hore, 1988; Kalaska et al. 1989; Crammond & Kalaska, 1996; Sergio & Kalaska, 1997). However, no studies have addressed this point specifically, so that the problem is unresolved.
The present results show that interhemispheric inhibition can interact with all three EMG bursts in the same way. Since the inhibition is thought to act at the motor cortex (e.g. Di Lazzaro et al. 1999) then the implication is that the motor cortex is involved in producing all three bursts. At first sight this conclusion differs from that reached by MacKinnon & Rothwell (2000). In that study, TMS pulses were applied to the motor cortex contralateral to the hand movement to evoke muscle responses at different times relative to the onset of EMG. Cortical excitability increased about 10–20 ms prior to the onset of AG1, but not before ANT. They suggested that ANT might be initiated by non-cortical mechanisms, perhaps involving cerebellar output to brainstem–spinal pathways. One way of reconciling these conclusions is to propose that tonic cortical outflow is needed to maintain the excitability of a non-cortical system that actually produces the EMG burst: withdrawal of this leads to a pause in activation. Another possibility is that corticospinal excitability to ANT is already high prior to ANT, so that the onset of ANT coincides exactly with increased cortical output with no lag between changes in cortical and spinal excitability.
Interactions between EMG bursts revealed by the ipsilateral silent period
The general rules for interactions between any individual EMG burst and the silent period can be summarized as:
The situation in (i) in which the silent period delays the onset of the EMG burst is similar to the effect observed by Day et al. (1989) when they stimulated contralateral cortex. In both cases, the TMS pulse causes a delay that affects not only the targeted EMG burst, but also all the subsequent bursts. Thus, a delay in onset of AG1 causes the whole triphasic EMG pattern to be shifted in time by the same amount whilst preserving the relative timing of the bursts and most of the movement parameters. Similarly a delay in onset of ANT also delays the onset of AG2. The conclusion is that the commands for movement must be stored in some way during the duration of the pause, and released when the motor cortex is ready to respond. Interestingly, the duration of the targeted burst is usually slightly shorter than normal and its amplitude larger. It may be that synchronization of cortical activity at the end of the silent period facilitates initiation of the burst. When AG1 is delayed this increase in amplitude leads to overshoot of the intended end position; if the ANT is delayed the effect on movement is less clear since the TMS pulse may also lead to early termination of AG1 (see below).
The situation in (ii) in which the silent period interrupts the targeted EMG burst usually has the same effect on the form of the triphasic pattern, i.e. all subsequent bursts are delayed. The total burst amplitude is also larger than normal, again perhaps because of synchronization of cortical activity after the silence. However, a subset of the data, equivalent to that described in section 2b of Results (‘Effects of TMS pulse just after onset of AG1’) shows different effects on AG1 and ANT. In this case, the TMS pulse was given about 5–8 ms after onset of the respective EMG burst with the silent period starting about 30 ms afterwards. In the case of AG1, the burst was interrupted by the silent period as expected, but ANT was not delayed. In addition, the duration of ANT was prolonged. The effect was to disrupt the temporal coordination of the triphasic pattern. A similar effect on the relation between ANT and AG2 was seen if the TMS pulse was given shortly after the onset of ANT, but the data to support this are slightly weaker.
Focusing attention on the relationship between AG1 and ANT, one explanation is that the time of onset of ANT is linked to activity in the first 35 ms, but not in later parts of AG1. Thus, if the silent period coincided with the first 30 ms of AG1, as in section 2a of Results (‘Effects of TMS pulse just before the onset of AG1’), ANT was delayed appropriately for the effect on AG1 (i.e. an increase in its duration); if the silent period began 35 ms into AG1, then ANT was not delayed. This effect would be compatible with the idea that a signal in the first 30–40 ms of AG1 initiates a process that eventually starts the ANT burst. For example, the cortex may send a message to cerebellum in this period to calculate the optimal onset latency of ANT according to the parameters of movement. Interruption of AG1 after this time cannot affect the onset of ANT since the message has already been sent. A similar argument can be put forward to account for the analogous effects on the relation between ANT and AG2.
In its simplest form this explanation would not account for the increase in duration of ANT in the case of interrupted AG1, non-delayed ANT: if the ANT burst were initiated as usual then its form would be expected to be unchanged. A confounding factor may be that in this condition, the onset of ANT overlaps AG1 far more then usual. If there were an interaction between these bursts (perhaps within the cortex), this might explain the changed form of ANT. For example, it has been proposed that there are reciprocal inhibitory connections between the outputs to antagonist muscles in cortex. If these were active in a ballistic movement, then the long AG1 might reduce the amount of activity at the start of the ANT; removal of this inhibition could lead to a rebound facilitation of ANT that prolonged the burst.
The situation in (iii) leads to early termination of the targeted EMG burst. The effect is different from those in (i) and (ii) since there is no compensation for the reduced amount of EMG caused by early termination. The conclusion is that the commands for the duration of the EMG burst are no longer stored during the pause in activity. In terms of the effect on AG1 we speculate that once the signal initiating ANT has been sent, then the remainder of the AG1 burst is no longer monitored. In fact, at this point in time, the main effect of the silent period moves to delaying the next EMG burst and the cycle begins again. A model to account for the data is given in Fig. 5.
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Footnotes |
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Bernd-Ulrich Meyer died on 24 November 2001.
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References |
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