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The Journal of Physiology logoLink to The Journal of Physiology
. 2004 Sep 23;561(Pt 1):307–320. doi: 10.1113/jphysiol.2004.069328

The effect of sensory input and attention on the sensorimotor organization of the hand area of the human motor cortex

Karin Rosenkranz 1, John C Rothwell 1
PMCID: PMC1665339  PMID: 15388776

Abstract

Sensory input can remodel representations in the sensory cortex, and this effect is heavily influenced by attention to the stimulus. Here we ask whether pure sensory input can also influence the spatial distribution of sensory effects on motor cortical hand area (sensorimotor organization) and whether this is modulated by attention. Sensorimotor organization was tested by applying short (1.5 s) periods of low amplitude vibration to single intrinsic hand muscles and measuring motor cortex excitability with transcranial magnetic stimulation (TMS). In healthy subjects, sensorimotor organization in the hand is focal, with input from one hand muscle increasing motor-evoked potentials (MEPs), decreasing short and increasing long-interval intracortical inhibition (SICI and LICI) in the vibrated muscle (‘homotopic’ effects) and having opposite effects on neighbouring muscles (‘heterotopic’ effects). Here we show that a 15 min intervention of vibration applied simultaneously to two hand muscles can lead to long-term (> 30 min) changes in the spatial pattern of sensorimotor interaction. The amount and direction of the effects depended on the subject's attention during the intervention: if subjects attended to both muscles when they were receiving simultaneous vibration, subsequent short-term vibration applied to one of them produced ‘homotopic’ effects on both muscles. ‘Heterotopic’ effects on a muscle not vibrated during the intervention were unaffected. If subjects did not attend to simultaneous vibration, subsequent short-term vibration of the muscles involved in the intervention no longer had any effect on them although the ‘heterotopic’ effects on a muscle not involved in the intervention were unchanged. We conclude that a 15 min period of pure sensory input can remodel the way that subsequent sensory inputs interact with motor output, that the effects are specific for the motor output to muscles involved in the intervention and that they are modulated by the subject's attention.

Many studies on experimental animals and humans have shown that somatosensory representations are remodelled by long periods of repeated sensory input. The changes depend on the spatial and temporal properties of the stimulus (Clark et al. 1988; Allard et al. 1991; Mogilner et al. 1993; Wang et al. 1995; Sterr et al. 1998; Ziemus et al. 2000) as well as the behavioural relevance and context (Jenkins et al. 1990; Xerri et al. 1996, 1999). Furthermore, the attentional demand during stimulation is important and determines the intensity/strength and direction of changes (Recanzone et al. 1992a,b; Noppeney et al. 1999; Braun et al. 2000, 2002).

The question we ask here is, can a period of pure repeated sensory input – in addition to changing the organization of the primary somatosensory cortex – also influence the pattern of sensorimotor interaction in the motor cortex? Indeed, there is good evidence in humans that periods of pure sensory stimulation can have after-effects on the excitability of the primary motor cortex (Hamdy et al. 1998; Ridding et al. 2000, 2001; Kaelin-Lang et al. 2002; Charlton et al. 2003), but the effect on sensorimotor interactions in the motor cortex has not been addressed nor has the role of attention.

In a previous paper (Rosenkranz & Rothwell, 2003) we introduced a technique to probe how sensory input interacts with motor output in the hand area of the human motor cortex. We showed that sensory input from short periods (1.5 s) of isolated muscle vibration affected the pattern of excitability in circuits controlling output to the vibrated as well as nearby muscles. The excitability of corticospinal and corticocortical projections to the vibrated muscle increased during the period of vibration whereas the excitability of areas controlling the other intrinsic muscles was suppressed. These changes were evident both in the amplitude of the motor-evoked potentials (MEPs) evoked by single-pulse TMS, as well as in the excitability of local inhibitory circuits investigated by paired-pulse TMS methods (SICI, short-interval intracortical inhibition, and LICI, long-interval intracortical inhibition). Since the latter are thought to test GABAergic circuits within motor cortex (Ziemann et al. 1996; Ilic et al. 2002) the implication was that sensory input from isolated muscle vibration had a highly organized pattern of connectivity to neural circuits in the hand area of motor cortex. We refer to this pattern as the baseline sensorimotor organization of the motor cortex.

In the present experiments we tested whether it was possible to modulate this baseline pattern by applying long periods of sensory input to the hand. The long-term stimulus consisted of vibration applied discontinuously for 15 min (2 s of vibration interleaved with 2 s rest) to a pair of intrinsic hand muscles, either with or without a concurrent attentional task. The effect of this intervention was followed up for 30 min by measuring the sensorimotor organization.

Methods

Subjects

Six healthy right-handed subjects (1 female) aged 26–32 years gave informed consent to the study, which was approved by the joint ethics committee of the Institute of Neurology and National Hospital for Neurology and Neurosurgery, London. All experiments conform to the Declaration of Helsinki. Subjects were comfortably seated in an armchair with their right forearm pronated and their hand relaxed on an armrest.

Transcranial magnetic stimulation

Transcranial magnetic stimulation (TMS) was performed using two MAGSTIM 200 stimulators connected to a figure-of-eight-shaped coil with an internal wing diameter of 7 cm by a Y-cable (Magstim, Dyfed, UK). The coil was held with the handle pointing backwards and laterally approximately 45 deg to the interhemispheric line to evoke anteriorly directed current in the brain and was optimally positioned to obtain motor-evoked potentials (MEPs) in the first dorsal interosseus muscle (FDI). The active motor threshold (aMT), defined as the minimum intensity needed to evoke a MEP of > 200 μV in 5 out of 10 trials, was measured in the slightly activated FDI. Stimulation intensities are quoted in the text as a percentage of maximal stimulator output (± s.e.m.) or percentages of aMT (± s.e.m.).

EMG recording

Surface electromyographic (EMG) recordings in a belly-to-tendon montage were made from the abductor pollicis brevis (APB), the first dorsal interosseus (FDI) and the abductor digiti minimi (ADM) muscle. The raw signal was amplified and filtered with a band pass filter of 30 Hz to 1 kHz (Digitimer Ltd). Signals were digitized at 2 kHz (CED Power1401, Cambridge Electronic Design, Cambridge, UK) and stored on a laboratory computer for off-line analysis.

Muscle vibration

Two electromechanical vibrators (Ling Dynamics System Ltd, UK), each with a 0.7 cm diameter probe, were used to apply vibration to the muscle belly of the FDI and APB muscles at a frequency of 80 Hz. The amplitude of vibration was adjusted separately in each individual so that it was just below the threshold for perceiving an illusory movement (Gilhodes et al. 1986; Roll et al. 1989; Roll & Gilhodes, 1995; Grunewald et al. 1997) and was in each case within a range of 0.2–0.5 mm. We monitored EMG in the vibrated muscle continuously for any signs of muscle contraction that might reflect either possible voluntary movement or occurrence of the tonic vibration reflex (Lance et al. 1966; Hagbarth & Eklund, 1968; Marsden et al. 1969). The amplitude and frequency of vibration were the same for short periods of single muscle vibration as they were for the long-lasting simultaneous vibration (see below).

It should be noted that muscle vibration, even of such small amplitude may potentially spread to parts of the hand other than those directly under the vibration probe. However, as we have shown before (Rosenkranz & Rothwell, 2003), the effect of vibration on MEP/SICI/LICI recorded in the hand muscles is highly dependent on the site where vibration is applied. We conclude that low-amplitude vibration produces a spatially significant gradient of afferent activation that can distinguish, for example, vibration of APB from vibration of FDI.

Experimental parameters

The measures were designed to explore the distribution of sensory effects on motor cortical projections to the three hand muscles using our previously described protocol (Rosenkranz & Rothwell, 2003). This involved measuring, with and without short-term vibration of the FDI or APB muscle (No Vib; Vib FDI; Vib APB), the peak-to-peak amplitude of MEPs after a single TMS pulse as well as short- and long-interval intracortical inhibition (SICI and LICI, respectively) using a subthreshold or supratheshold conditioning stimulus (Kujirai et al. 1993; Berardelli et al. 1996). These parameters were tested in two consecutive experimental blocks, with block 1 consisting of MEPs in response to a single TMS pulse and SICI, and block 2 of LICI only.

Block 1: MEP and SICI

These parameters were measured in a randomized paired-pulse design using an interstimulus interval (ISI) of 3 ms. The test stimulus intensity (SI) was adjusted to give an MEP of approximately 1 mV peak-to-peak (SI 1 mV) in the relaxed FDI muscle and the intensity of the conditioning stimulus set so as to produce about 50% inhibition. We adjusted the conditioning intensity to produce 50% SICI in the following way: we started with an intensity of 80% aMT, and if the SICI was stronger than 50%, the conditioning stimulus intensity was reduced; if it was less than 50% the conditioning stimulus intensity was increased. Single (test pulse alone) or pairs of pulses were applied randomly every 5 s. Stimuli were applied in the presence of FDI vibration, APB vibration or without vibration, one-third of the trials for each condition. Vibration was applied for 1.5 s (here called ‘short-term’), starting 1 s before the TMS test pulses were applied. A total of 60 trials were collected with 10 trials of each condition. Our previous study (Rosenkranz & Rothwell, 2003) showed that 10 trials of each condition give a reasonable compromise between practicability and the expected physiological variability of the results. The variability of results obtained here was within a range described for these TMS parameters by Orth et al. (2003). The peak-to-peak amplitude of the MEPs evoked in each of the three hand muscles was measured on each single trial so that the mean amplitude and percentage SICI for the three vibration conditions could be calculated.

Block 2: LICI

LICI was tested with a suprathreshold conditioning stimulus delivered 100 ms before the test stimulus as described in previous studies (Nakamura et al. 1997; Chen et al. 1999). The stimulus intensities of the conditioning and test stimuli were the same and set at SI 1 mV. Thirty paired-pulse TMS stimuli were presented and randomized between each of the following conditions: no vibration, during short-term vibration of APB, or during short-term vibration of FDI as in block 1.

It should be noted that although short-term vibration increases the amplitude of the test MEP, we have previously shown that the percentage SICI and LICI is unaffected by variations in MEP amplitude over this range (Rosenkranz & Rothwell, 2003). Therefore, an adjustment of the test pulse intensity to evoke MEPs of matching size (1 mV peak-to-peak amplitude) was not necessary.

Intervention: long-lasting simultaneous vibration

Simultaneous vibration lasted 15 min and involved repeated cycles of vibration (2 s on, 2 s off) applied to both the APB and FDI. Subjects completed this experiment on two separate occasions. On one they were asked to perform a frequency attention task, whereas in the other they were not attending to the vibration.

Intervention 1: long-lasting simultaneous vibration with a concurrent frequency attention task (‘attention task’)

In 60% of trials at random the frequency of vibration applied to one of the muscles was changed from 80 Hz to 65, 70 or 75 Hz for the last 300 ms of the train. Subjects had to indicate in the 2 s rest period between vibration cycles whether they perceived a change in the APB, or in the FDI or no change at all by pressing the corresponding buttons on a response box with their left hand. Subjects were instructed to be as accurate rather than as quick as possible. Feedback of whether their answer was correct or not was given after each trial. The responses were digitized at 100 Hz (CED Power1401) and stored on a laboratory computer for off-line analysis.

Intervention 2: long-lasting passive simultaneous vibration (‘passive condition’)

In the passive condition the vibration frequency did not change in either muscle. Subjects received simultaneous vibration of the APB and FDI (2 s on, 2 s off) for 15 min. They were instructed not to pay attention to the stimulus and either read or listened to music during this time. The lack of change in vibration frequencies made this condition slightly different to intervention 1. Although the vibration was a very subtle stimulus and easy to neglect, we wanted to make sure that subjects' attention was not drawn to the vibration if there were slight changes in frequency, thus we kept frequencies equal throughout.

Protocol

Each subject participated in two experiments (intervention 1 and intervention 2 in a randomized order and at least 1 week apart). In both of them, we tested the sensorimotor organization in intrinsic hand muscles before and after the intervention. MEPs and SICI (block 1) and LICI (block 2) were tested before the intervention (baseline), directly after (t0), and 15 (t15) and 30 min (t30) after the end of the intervention. Each set of testing of blocks 1 and 2 took about 7.5 min altogether, which allowed a rest between the TMS blocks, in which the subject remained seated with the hand and forearm relaxed on the armrest.

Data analysis and statistics

The intensities of the conditioning and the test stimuli (SI 1 mV), given as a percentage of stimulator output or of aMT (± s.e.m.), were compared between the two experimental parts (‘attention task’ and ‘passive condition’) by means of paired t tests.

The peak-to-peak amplitudes of single-pulse MEPs without and during short-term vibration of a single muscle are given as raw data (mV ± s.e.m.). For SICI, single trial peak-to-peak MEP amplitudes were measured and averaged and their size expressed as a percentage of the mean test MEP. LICI was expressed as the ratio of conditioned/test MEP size within a trial.

For all TMS parameters several repeated measures ANOVA were performed as follows. A three-way ANOVA was performed with the factors ‘muscle’, ‘time course’ (i.e. before and at the three time points after the intervention) and ‘vibration condition’ (i.e. no vibration, short-term vibration of APB, short-term vibration of FDI) separately for each of the attention conditions (‘attention task’ and ‘passive condition’). Further two-way analysis was undertaken for the data measured in each hand muscle separately by testing the interaction of the factors ‘time course’ and ‘vibration condition’. A one-way ANOVA was finally performed to test the influence of the factor ‘time course’ on the data measured in the APB and FDI muscles with short-term APB or FDI vibration (see Tables 1 and 2). Where necessary, post hoc t tests were performed (as indicated in Results).

Table 1.

Part of the three-way ANOVA on the data from subjects who were given simultaneous vibration with a concurrent attention task

ANOVA Main factor(s) Degrees of freedom; error MEP SICI LICI
F P F P F P
3-way Muscle × time course × vibration condition 12; 60  11.60 < 0.0001 20.04 < 0.0001 12.33 < 0.0001
2-way Time course × vibration condition 6; 30
 APB 7.36 < 0.0001 17.40 < 0.0001 13.88 < 0.0001
 FDI 10.07 < 0.0001 33.62 < 0.0001 10.97 < 0.0001
 ADM* 0.96 n.s. 0.49 n.s. 0.35 n.s.
2-way Muscle × time course 6; 30
 No Vib** 0.88 n.s. 0.98 n.s. 1.34 n.s.
 Vib APB 9.98 < 0.0001 22.66 < 0.0001 12.59 < 0.0001
 Vib FDI 6.78 < 0.0001 14.47 < 0.0001 16.96 < 0.0001
1-way Time course   3; 15
 APB with Vib APB 1.29 n.s. 2.21 n.s. 5.95 < 0.01
 APB with Vib FDI 10.48 < 0.01 57.73 < 0.0001 15.36 < 0.01
 FDI with Vib APB 11.93 < 0.01 63.51 < 0.0001 11.36 < 0.01
 FDI with Vib FDI 1.05 n.s. 1.11 n.s. 0.59 n.s.
*Main effect of time course 3; 15 0.31 n.s. 0.49 n.s. 0.32 n.s.
**Main effect of time course 1.25 n.s. 2.25 n.s. 0.56 n.s.
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The six columns on the right show results separately for the analysis of motor-evoked potentials (MEPs), and short- and long-interval intracortical inhibition (SICI and LICI). Each row gives the F and associated P value for a particular main factor or interaction term in the ANOVA. The first row shows the three-way interaction between ‘muscle’, ‘time course’ and ‘vibration condition’. The three following rows show the results of the follow-up two-way analysis on each muscle separately with ‘time course’ and ‘vibration condition’ as main factors. The next three rows show a follow-up two-way ANOVA on each vibration condition separately with ‘time course’ and ‘muscle’ as main factors. The next four rows are the remaining one-way ANOVAs with ‘time course’ as the main factor on data from abductor pollicis brevis (APB) and first dorsal interosseus (FDI) muscles during vibration of either APB or FDI. Degrees of freedom associated with each set of comparisons are given for each set of ANOVAs. The last two rows show the statistics for the main effect of ‘time course’ in the two-way ANOVAs for the abductor digiti minimi (ADM) muscle and the no vibration condition. n.s., not significant.

Table 2.

Part of the three-way ANOVA on the data from subjects who were given passive simultaneous vibration

ANOVA Main factor(s) Degrees of freedom; error MEP SICI LICI
F P F P F P
3-way Muscle × time course × vibration condition 12; 60 4.31 < 0.0001 10.07 < 0.0001 5.10 < 0.0001
2-way Time course × vibration condition  6; 30
 APB 2.01 n.s. 6.93 < 0.0001 3.55 < 0.01
 FDI 3.82 < 0.01 7.81 < 0.0001 5.66 < 0.01
 ADM* 1.10 n.s. 0.77 n.s. 0.75 n.s.
2-way Muscle × time course  6; 30
 No Vib** 1.83 n.s. 0.81 n.s. 1.08 n.s.
 Vib APB 2.09 n.s. 10.28 < 0.0001 5.14 < 0.01
 Vib FDI 4.07 < 0.01 6.52 < 0.01 3.70 < 0.01
1-way Time course 3; 15
 APB with Vib APB 1.87 n.s. 8.85 < 0.01 1.89 n.s.
 APB with Vib FDI 2.98 n.s. 2.93 n.s. 3.15 n.s.
 FDI with Vib APB 1.71 n.s. 4.87 < 0.05 4.96 < 0.05
 FDI with Vib FDI 3.39 < 0.05 4.19 < 0.05 2.18 n.s.
*Main effect of time course  3; 15 0.62 n.s. 3.44 0.04 0.3 n.s.
**Main effect of time course 2.14 n.s. 2.73 n.s. 1.53 n.s.
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For further details refer to legend of Table 1.

To test for the influence of attention, the data set was simplified: we calculated the difference between the amplitudes of MEPs, SICI and LICI measured without vibration and during short-term vibration of APB or FDI before and after the intervention vibration for each of the attention conditions (‘attention task’ and ‘passive condition’). The data from the three time points after the intervention have been averaged to provide a single value. The baseline data are the mean of the two experiments. Two-tailed paired t tests were calculated for each TMS parameter within each vibration condition (short-term vibration of APB or FDI). The data are displayed in Fig. 5, where the statistical results are indicated.

Figure 5. Simultaneous vibration of APB and FDI: comparison of the results after intervention 1 (attention task) and intervention 2 (passive condition).

Figure 5

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Left and right panels show data from APB and FDI, respectively, while the three rows show measures of MEP amplitude and percentage SICI and LICI. Each column plots the difference between the data obtained without vibration and data collected during short-term vibration of APB (grey columns) and FDI (black columns). For example, at baseline, short-term vibration of APB increased MEPs in APB by a mean of about 0.5 mV, whereas short-term vibration of FDI decreased MEPs by 0.3 mV. The data from the three time points after the interventions have been averaged to provide a single value. The size of the effects following interventions with discrimination (attention) and passive vibration (passive) were compared using paired t tests. Data are means ± s.e.m. *P < 0.05, **P < 0.0001.

The behavioural data are given as number of mistakes (± s.e.m.) per minute and the effect of task duration on the number of mistakes was analysed with a repeated-measures ANOVA with the factor ‘task duration’. The significance level was set at P < 0.05.

Results

No subjects experienced any side-effects of the TMS testing during these experiments. The intensity of the test stimulus (attention task: 39 ± 2% stimulator output; passive condition: 38 ± 1%) and the intensity of the conditioning stimulus (attention task: 21 ± 2% stimulator output, 79 ± 2% of aMT; passive condition: 23 ± 2% stimulator output, 82 ± 2% of aMT) was not significantly different in the two experimental conditions.

Intervention 1: long-lasting simultaneous vibration with a concurrent attention task (‘attention task’)

Figure 1 displays the number of mistakes per minute (± s.e.m.) made by the subjects during the 15 min of the vibration frequency discrimination task. The number of mistakes did not change significantly over time (ANOVA; F14; 56= 1.16; P = 0.33) suggesting that subjects maintained a constant level of attention throughout the task.

Figure 1. Average number of mistakes (maximum 15) made per minute during the frequency discrimination task.

Figure 1

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The task duration had no significant effect on the number of mistakes made per minute (ANOVA (‘task duration’), n.s). Data are means ± s.e.m.

Figure 2 shows examples of original MEP recordings in all hand muscles after a single TMS pulse. Each trace shows the responses with and without short-term vibration of APB or FDI. Figure 2A displays the distribution of effects on the MEPs in the different hand muscles before the intervention: vibration of one hand muscle facilitates the MEP in the vibrated, but suppresses the MEPs in the non-vibrated muscles. Figure 2B shows the same parameters measured 30 min after the intervention: short-term vibration of the APB or the FDI now facilitates the MEPs in both muscles, whereas the MEPs in the ADM are still suppressed.

Figure 2. Average EMG recordings from hand muscles of one representative individual.

Figure 2

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Traces show how motor-evoked potentials (MEPs), evoked without vibration (No Vib), are affected by applying short periods of vibration to abductor pollicis brevis (APB) or first dorsal interosseus (FDI) muscles (Vib APB or Vib FDI). A, baseline effects prior to long-lasting simultaneous vibration. Vibration increases MEPs in the vibrated muscle, while suppressing those in the non-vibrated hand muscles. B, results obtained 30 min after long-lasting (15 min) vibration was applied simultaneously to FDI and APB while subjects performed a discrimination task. Vibration of either APB or FDI now increased MEPs in both muscles, whereas those in abductor digiti minimi (ADM) were still suppressed. C, results obtained 30 min after long-lasting (15 min) simultaneous vibration in the passive condition where subjects paid no attention to the stimulus. In contrast to the attention condition, vibration of APB or FDI had no effect on MEPs in either muscle even though MEPs in ADM were still suppressed.

Figure 3 illustrates the effect of the intervention on the three measures of motor cortical excitability (i.e. MEP amplitude, SICI and LICI) in each of the three hand muscles (APB, FDI, ADM). Each set of histograms plots the data from before, and at three time points after, the 15 min intervention. Finally, the columns are plotted in triplets to show (i) the value of the measure (MEP, SICI, LICI) without vibration (open columns), (ii) the value during short-term vibration of APB (grey columns), and (iii) the value during short-term FDI vibration (black columns). The difference between values without vibration and values during short-term vibration is a measure of the spatial distribution of sensory effects from the vibrated muscle.

Figure 3. The effect of long-lasting simultaneous vibration with a concurrent discrimination task on sensorimotor organization.

Figure 3

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Each column of graphs shows data from one of the three intrinsic hand muscles (APB, FDI, ADM). Each row shows the effect on a different measure of motor cortical excitability (MEP, short-interval intracortical inhibition (SICI), long-interval intracortical inhibition (LICI)). MEP is measured in millivolts peak-to-peak; SICI and LICI are expressed as percentage inhibition relative to unconditioned control values. Four time points have been plotted for each measure: baseline, and directly (t0), 15 min (t15) and 30 min (t30) after the end of the intervention. Each set of three histogram bars shows data obtained without vibration (open columns), data collected during short-term vibration of APB (grey columns), and data collected during short-term vibration of FDI (black columns). At baseline, short-term muscle vibration produced a differential effect on vibrated versus non-vibrated muscles. The intervention abolished this difference in FDI and APB. Data are means ± s.e.m.

The baseline organization before the intervention was the same as previously described (Rosenkranz & Rothwell, 2003). Short-term (1.5 s) vibration of FDI or APB produced homotopic effects in the vibrated muscle consisting of: (i) increased MEPs, (ii) decreased SICI, and (iii) increased LICI. Heterotopic effects in the non-vibrated muscles had the opposite sign. For example, APB vibration increased MEPs in APB but reduced them in FDI and ADM. Conversely, FDI vibration increased MEPs in FDI but decreased them in APB and ADM.

The 15 min period of simultaneous vibration had no effect on levels of MEP, SICI or LICI measured without vibration. However, there was a clear change in how these measures were affected by sensory inputs. After the intervention, FDI and APB muscles, instead of responding oppositely to short-term vibration applied to either one or other muscle, now responded in the same way. Effectively, the homotopic effects produced by short-term FDI vibration in the FDI muscle were now observed in APB and vice versa. The heterotopic effects on the ADM muscle were unchanged.

These features were confirmed in the statistical analysis (Table 1) of MEP, SICI and LICI. A three-way ANOVA conducted separately on each measure, with ‘muscle’, ‘time course’ and ‘vibration condition’ as main factors, revealed a significant three-way interaction for all three measures. The influence of the factor ‘muscle’ was explained by the fact that the effects in ADM did not change after the intervention whereas they did in the two other muscles. This was confirmed in subsequent two-way analyses for each muscle separately. There was a significant ‘time course’ and ‘vibration condition’ interaction for all measures in APB and FDI. In ADM there was no significant interaction or a main effect of the factor ‘time course’.

The influence of the factor ‘vibration condition’ in the three-way interaction was explained by the fact that there was no difference in the measures taken without vibration before and after the intervention, whereas there was a clear difference in the measures made during short-term vibration of a single muscle. Thus when each vibration condition was analysed separately in a two-factor ANOVA, there was a significant interaction between ‘muscle’ and ‘time course’ only in the conditions in which MEPs, SICI and LICI were measured during short-term vibration of a single muscle. In the no vibration condition there was no significant interaction or main effect of ‘time course’.

Since the ADM and the no vibration condition showed no significant effects, we concentrated the remainder of the analysis on ‘time course’ data from the APB and FDI muscles measured during single muscle vibration (see Table 1). Short-term vibration of the APB had the same effect on MEPs and SICI measured in the APB before and after the patterned simultaneous vibration (i.e. no significant main effect of ‘time course’). Conversely, in FDI, the effects of APB vibration were significantly affected by the factor ‘time course’, with post hoc testing showing that the only significant pairwise comparisons involved results collected before versus after the intervention. A similar pattern was seen for parameters measured in the FDI muscle: those measured during single muscle vibration of FDI did not change whereas those measured during single muscle vibration of APB did change.

Intervention 2: long-lasting passive simultaneous vibration (‘passive condition’)

Examples of original MEP recordings in all hand muscles after 15 min of passive simultaneous vibration are shown in Fig. 2C. MEPs in APB and FDI are no longer modulated by short-term vibration of either FDI or APB whilst the MEPs in ADM are still suppressed.

Figure 4 has the same format as Fig. 3 and shows the effect on MEPs, SICI and LICI before and after the intervention. The graphs show again that the intervention had no effect on levels of MEP, SICI and LICI made without vibration. However, there was a clear change in the way these measures were influenced by short-term vibration of a single muscle, particularly at the first time point after the end of the intervention. For example, in the baseline state, short-term vibration of APB or FDI had opposite effects on the MEP in APB. After the intervention, short-term vibration of either muscle no longer appeared to have any effect compared to the no vibration condition. In the last measurement 30 min after the end of the intervention, the effect of short-term APB and FDI vibration reappeared, at least for some of the parameters. To summarize, when subjects did not have to attend to the vibration during the 15 min intervention, the subsequent effect of short-term vibration of a single muscle on MEPs, SICI and LICI was attenuated, at least in the two muscles that had received the vibration during the intervention. In contrast, the heterotopic effects of vibration applied to either APB or FDI on measures in ADM were unchanged.

Figure 4. The effect of long-lasting passive simultaneous vibration of APB and FDI on sensorimotor organization.

Figure 4

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Data are displayed as in Fig. 3. The differential effect of short-term muscle vibration on vibrated versus non-vibrated muscles at baseline is attenuated after the intervention. Data are means ± s.e.m.

As for the results after simultaneous vibration with attention task, a three-way ANOVA with ‘muscle’, ‘time course’ and ‘vibration condition’ as main factors revealed a significant three-way interaction for all measures (Table 2). Since the influence of the factors ‘muscle’ and ‘vibration condition’ were explained, as above, by the fact that the intervention had no effect on (1) any of the measures in ADM whilst it did in the other two muscles, or (2) the measures in the no vibration condition, we focus the remainder of the analysis on the ‘time course’ of measures made during short-term vibration of FDI or APB. Table 2 shows that there was a small effect of ‘time course’ on some but not all of the measures in both muscles. To help understand this further we then made, for the FDI and APB data, post hoc comparisons between the (usually opposite) effects of single muscle vibration of FDI and vibration of APB. These showed that the significant baseline difference between measurements made during short-term vibration of APB or FDI (paired t test; P < 0.01) disappeared directly after the intervention. The differential effect had returned 15 min after intervention in APB MEP and additionally 30 min after intervention in FDI MEP and APB LICI (paired t test; P < 0.05).

Comparison of intervention 1 and intervention 2

Since the results of these two sets of experiments were the same in the ADM muscle, we confined this analysis to the APB and FDI muscles. The data are illustrated in Fig. 5 where we have plotted the difference between the amplitudes of MEPs, SICI and LICI measured without and with short-term vibration of APB or FDI before and after the interventions. In these graphs, the data from the three time points after the interventions have been averaged to provide a single value. The baseline data are the mean of the two experiments.

The graphs show that as previously described (Rosenkranz & Rothwell, 2003) at baseline short-term vibration of APB had opposite effects to those seen during short-term FDI vibration (the grey and the black columns extend in opposite directions). After the intervention, short-term vibration of either muscle had similar effects (the grey and black columns are more likely to extend in the same direction). The results also show that if subjects had to attend during the intervention, then the effects of short-term vibration of a single muscle were larger than those seen after the passive condition (paired t tests are shown in the figure).

Discussion

The present experiments showed that a 15 min period of simultaneous hand muscle vibration can change the spatial distribution of sensory inputs to motor cortex for up to 30 min afterwards. The effects depend on whether subjects attend to the vibration during the period of application. Figure 6 summarizes the results diagrammatically.

Figure 6. Schematic summary of the effects of focal vibratory input on SICI and LICI in the three hand muscles.

Figure 6

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In this diagram, the hand muscle representations are drawn as circles with the vibrated muscle (either APB or FDI) in the centre, and the ‘near’ (either FDI or APB) and ‘far’ (always ADM) non-vibrated muscles surrounding it. Shades represent the level of intracortical inhibition: white symbolizes a reduction of SICI or LICI, grey an increase, and patterned, an unchanged SICI or LICI compared to the non-vibration condition. Before the intervention (baseline), short-term vibration of one muscle reduces SICI in that muscle (‘homotopic’ effect) and increases it in other muscles (‘heterotopic’ effect), as symbolized here by the white centre surrounded by grey for SICI, and vice versa for LICI. After the long-term simultaneous vibration of the APB and FDI, the ‘homotopic’ effect of vibration spreads onto the co-vibrated muscle if subjects had attended to the vibratory stimulus (attention task). If subjects did not attend, vibration of either FDI or APB no longer had any effect on FDI or APB. The ‘heterotopic’ effects of short-term APB or FDI vibration on the ADM are preserved.

Locus of change in CNS

The method we used to describe the pattern of sensory influence on motor cortex employed three measures of motor cortex excitability (MEP amplitude, SICI and LICI). These were tested in three different intrinsic hand muscles (FDI, APB and ADM) and compared in the presence or absence of short-term (1.5 s) vibration applied to the muscle belly of either FDI or APB. Vibration of one muscle had opposite effects on MEP, SICI and LICI in the vibrated and non-vibrated muscles. Since SICI is believed to test the excitability of intrinsic circuits in motor cortex (Di Lazzaro et al. 1998), any effects on SICI must occur because sensory input modulates the excitability of motor cortex circuits. The same is probably true for LICI and MEPs although these two measures are also affected by the excitability of spinal cord circuits (Chen et al. 1999; Kossev et al. 1999). This may explain some of the apparent differences in behaviour of the three parameters in follow-up 1- and 2-way ANOVAs (see Table 1: 1-way ANOVA ‘APB with Vib APB’; Table 2: first 2-way ANOVA ‘APB’ and second 2-way ANOVA ‘Vib APB’).

The differential effect of short-term vibration on vibrated versus non-vibrated hand muscles appears to be unique to this sensory modality, since similar results have not been described in studies using cutaneous inputs (Classen et al. 2000; Tamburin et al. 2001). This may be because muscle vibration predominantly stimulates the Ia-afferents of muscle spindles (Burke et al. 1976a,b; Roll et al. 1989) whose input may have direct access to both sensory (area 3a) and motor (area 4) cortices (Heath et al. 1976; Hore et al. 1976; Jones & Porter, 1980). The latter may allow it to have more specific effects on motor cortical circuitry as summarized in a previous paper (Rosenkranz & Rothwell, 2003).

If our test of sensorimotor organization examines how sensory inputs activated by muscle vibration normally interact with the excitability of circuits in the motor cortex, then the changes that we see after applying a long period of simultaneous vibration must be due to long-term modification of these connections. This could have occurred because of changes in response of the sensory receptors to short-term vibration or because of changes in transmission of information to sensorimotor cortex. Although the former may occur transiently after long periods of stimulation (Jack & Roberts, 1974), it seems unlikely to account for the results we obtained since (i) the effect of single muscle vibration on the responses evoked in ADM remained the same, and (ii) the effects were modified by the level of the subject's attention.

It should be noted that in contrast to other studies which described an increase of motor excitability after prolonged cutaneous or mixed nerve stimulation (Hamdy et al. 1998; Ridding et al. 2000, 2001; Charlton et al. 2003) but no influence on intracortical inhibitory mechanisms (Stefan et al. 2002; Kaelin-Lang et al. 2002), none of the parameters measured without vibration (control values) were changed after the long-lasting simultaneous vibration. We conclude that the long period of vibration changed specifically the way in which subsequent vibratory input interacts with circuits in the motor cortex without increasing the level of motor excitability in general. The latter also had the practical technical advantage that we did not need to adjust the intensity of the stimulus parameters before and after long-term vibration.

Possible mechanisms of the after-effects of long-term simultaneous vibration

After long-term simultaneous vibration with attention, the usually opposite ‘homotopic’ and ‘heterotopic’ effects on MEPs, SICI and LICI disappeared in FDI and APB. Vibration applied to one of these muscles now produced the same ‘homotopic’ effect in both of them. In monkey and human studies a period of simultaneous stimulation to adjacent digits leads to overlap or even fusion of their representations in the sensory cortex (Clark et al. 1988; Allard et al. 1991; Wang et al. 1995; Ziemus et al. 2000). It is possible that the long period of simultaneous vibration to APB and FDI produced a similar effect in the present experiments perhaps fusing the sensory representations for each muscle. This might mean, for example, that sensory input from one muscle reaches the sensory representation of the other muscle, although we cannot say whether the changes occur only at the level of cortical sensory representations or also on representations at a subcortical level. Nevertheless, whatever the precise mechanism, FDI input could reach the motor output to APB via the sensory representation of APB, leading to typical ‘homotopic’ effects on APB. Effectively, reorganization of the sensory input might propagate to its output connections, with direct consequences for sensorimotor coupling. Interestingly, such a suggestion might also mean that the usual ‘heterotopic’ influences from FDI to APB are reduced.

Another possibility is that motor cortical circuits are directly influenced by the intervention. We have suggested previously that single muscle vibration modulates the excitability of GABAergic inhibitory circuits in the motor cortex (Rosenkranz & Rothwell, 2003). GABAergic inhibitory circuits are crucial to the dynamic process of map organization in the motor cortex and critically placed to maintain or readjust the form of cortical motor representations (Jacobs & Donoghue, 1991). An expansion of the ‘homotopic’ vibration effect after the intervention towards the co-stimulated muscle might therefore be due to an unmasking of pre-existing connections between muscle representations.

The present experiments cannot address whether one or both of these explanations is correct. Nevertheless, they do show that the sensory inputs can have a lasting influence on sensorimotor organization and that these can be induced within a very short time span.

Interestingly, the differential effect of muscle vibration on SICI and LICI as seen at baseline is consistent even after the interventions. If SICI is reduced then LICI is increased and vice versa. Both phenomena are thought to be due to activity in different cortical GABAergic circuits (Sanger et al. 2001) with LICI operating via GABAB mechanisms (Roick et al. 1993; Werhahn et al. 1999), whereas SICI involves the activation of short-lasting inhibitory GABAA mechanisms (Hanajima et al. 1998; Ilic et al. 2002). Both circuits interact, and LICI may suppress excitability in neurones responsible for SICI, perhaps via the activation of presynaptic GABAB receptors (Sanger et al. 2001). The persistence of the differential effect of short-term vibration on both inhibitory circuits after the interventions might imply (1) that changes induced by the intervention in one circuit drive the changes in the other, or (2) that the intervention influences the circuits independently and differently. It is not possible to answer this with the data presented here. Nevertheless, in functional terms we might speculate that the net effect is to maintain the overall level of inhibition in the motor cortex, whilst shifting the balance between different pathways.

Role of attention

In the present experiments the attention task was designed to force subjects to attend actively to the frequency of muscle vibration, whereas in the passive condition subjects did not pay attention to it. Although we did not have any control task to verify the lack of attention, the vibratory stimulus was very subtle and subjects reported no difficulty in cooperating with the instruction. The fact that the results were very different from the attention condition is consistent with this suggestion.

Previous animal work has shown that passive stimulation has little effect on the reorganization of sensory cortex compared to attended stimulation (Recanzone et al. 1992a,b). However, in the present experiments, the intervention with simultaneous passive vibration caused the ‘homotopic’ and ‘heterotopic’ effects of subsequent single vibration to attenuate, rather than remain unchanged. The results were selective for the co-vibrated muscles and did not influence the ‘heterotopic’ effect of single muscle vibration on other muscles (e.g. ADM). It was as if the principal circuits that had received long-term simultaneous vibration lost their response to single muscle vibration, effectively ‘filtering out’ subsequent inputs in the pathways activated during long-term simultaneous vibration. Similar observations have been made with recordings of an ex vivo network, which showed that neurones involved in processing frequent unattended stimuli selectively attenuated their responsiveness towards them (Eytan et al. 2003).

Unlike the results after the intervention with the attention task, however, the data cannot readily be explained by a ‘knock-on’ effect of sensory reorganization. Thus, we cannot suggest that the reduced ‘homotopic’ and ‘heterotopic’ effects on FDI and APB are due to reduced access of short-term vibration to the sensory representations of these muscles. If it were, and if sensorimotor interaction simply reflected connections between corresponding sensory and motor areas of cortex, then we would expect that the ‘heterotopic’ effects of FDI and APB vibration on ADM would also disappear. However, this was not the case: effects on ADM were unchanged. We conclude that the 15 min of non-attended vibration directly changed the effect of short-term vibration on the excitability of inhibitory motor cortical circuits.

Conclusion

The way vibratory input interacts with circuits responsible for SICI and LICI, as well as the change of this interaction after simultaneous muscle vibration of APB and FDI, is sketched in Fig. 6. We have chosen to illustrate the effects on SICI and LICI because of the possibility that non-cortical changes could contribute to the differences in spatial effects on the MEP. In this diagram, the hand muscles are displayed as concentric circles with the vibrated muscle (APB or FDI) in the middle, and the non-vibrated ‘near’ (APB or FDI) or ‘far’ neighbour (always ADM) surrounding it. Before the intervention, focal vibratory input to either APB or FDI reduces SICI in that muscle (‘homotopic’ effect) and increases it in other muscles (‘heterotopic’ effect); the changes in LICI are opposite. After the long-term simultaneous vibration of APB and FDI, the ‘homotopic’ effect of vibration spreads to the co-vibrated muscle if subjects attended to the vibratory stimulus (attention task). If subjects do not attend, the vibration of either FDI or APB has no effect on the FDI or APB muscles. The ‘heterotopic’ effects of short-term APB or FDI vibration on the ADM are preserved.

We conclude that pure sensory input can remodel the way that subsequent sensory inputs interact with motor output. The effect develops quickly (after only 15 min) and lasts for at least 30 min. Changes are specific for the motor cortical output to muscles that were vibrated during the intervention and are modulated by the subject's attention. We hypothesize that at least some of these effects are due to modifications in circuits of the motor cortex itself. The observations indicate that somatosensory input is important for representational plasticity in motor as well as sensory cortex. Finally, the fact that sensory inputs can modulate patterns of sensorimotor interactions may be relevant to understanding why some pathological forms of organization such as seen in patients with focal hand dystonia may be related to a history of repetitive activity in motor and sensory pathways (Byl et al. 1996; Elbert et al. 1998). Further experiments are needed to test whether specific properties of sensory stimulation (e.g. simultaneously versus non-simultaneously applied) influence the sensorimotor organization in a different way.

Acknowledgments

K.R. was supported by a research grant from ‘Deutsche Forschungsgemeinschaft’. The work was funded by the Medical Research Council.

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