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Differential modulation of the short- and long-latency somatosensory evoked potentials in a forewarned reaction time task
Clinical Neurophysiology 115 (2004) 2223–2230 www.elsevier.com/locate/clinph
Differential modulation of the short- and long-latency somatosensory evoked potentials in a forewarned reaction time task Tetsuo Kidaa,*, Yoshiaki Nishihirab, Toshiaki Wasakaa, Yukie Sakajiric, Toshiki Tazoec a
Doctoral program in Health and Sports Sciences, University of Tsukuba, Tsukuba, Japan b Institute of Health and Sports Sciences, University of Tsukuba, Tsukuba, Japan c Master’s program in Health and Sports Sciences, University of Tsukuba, Tsukuba, Japan Accepted 22 April 2004 Available online 25 June 2004
Abstract Objective: We investigated modulation of the short- and long-latency somatosensory evoked potentials (SEPs) in a forewarned reaction time task. Methods: A pair of warning (auditory) and imperative stimuli (somatosensory) was presented with a 2 s interstimulus interval. In movement condition, subjects responded by grip movement with the ipsilateral hand to the somatosensory stimulation when the imperative stimulus was presented. In counting condition, they silently counted the number of imperative stimuli. The SEPs in response to the imperative stimuli were recorded. Results: Frontal N30 and central N60 amplitudes were significantly smaller in the movement than in the counting or rest conditions. None of the short-latency components differed between the counting and rest conditions. In contrast to the short-latency components, P80 was significantly larger in the counting than in the rest condition, and showed a further increase from the counting to the movement condition. The N140 amplitude was significantly larger in the movement than the rest condition, but was not changed between the counting and the rest conditions. Conclusions: The attenuation of the frontal N30 and central N60, and the enhancement of the P80 and possibly the N140 resulted from the centrifugal mechanism. The present findings may show the different effects of voluntary movement on the early and subsequent cortical processing of the relevant somatosensory information requiring a behavioral response. Significance: The present study demonstrated the differential modulation of short- and long-latency components of SEPs in a forewarned reaction time task. q 2004 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. Keywords: Somatosensory evoked potentials; Centrifugal gating; Attention; Voluntary movement
1. Introduction Relevant somatosensory information is influenced in various ways at different processing stages. This modulation of somatosensory information can be studied by somatosensory-evoked potentials (SEPs). Many studies have shown an attenuation of short-latency SEPs which occurs when a stimulus is delivered during active movement (Cheron and Borenstein, 1987, 1991, 1992; Cheron et al., 2000; Cohen and Starr, 1987; Nishihira et al., 1991; Rossini et al., 1996, 1999; Waberski et al., 1999; Valeriani et al., 1999). In these * Corresponding author. Fax: þ 81-29-853-2607. E-mail address: [email protected] (T. Kida).
previous studies, however, a somatosensory stimulus to evoke the SEPs was irrelevant to the subject’s movement task. There have been some attempts to examine the effects of voluntary movement or movement preparation on the SEPs in response to relevant stimulus. These studies found an attenuation of the SEPs when subjects responded to the somatosensory stimuli to evoke the SEPs (Asanuma et al., 2003; Murase et al., 2000; Shimazu et al., 1999). However, they did not show the data of long-latency SEP components (such P80 and N140 components). It has been reported that long-latency SEPs were attenuated (Jones, 1981; Rushton et al., 1981) or enhanced (Bo¨cker et al., 1993; Hazemann et al., 1975; Lee and White, 1974; Nakata et al., 2003) during voluntary movement.
1388-2457/$30.00 q 2004 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2004.04.017
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Recently, Nakata et al. (2003) reported the enhancement of the long-latency components during active movement. In addition to these SEP studies, magnetoencephalography (MEG) studies have shown that the short-latency SI activities were attenuated before and during voluntary movement (Kakigi et al., 1995; Wasaka et al., 2003), whereas the long-latency SII activities were enhanced (Huttunen et al., 1996; Forss and Jousmaki, 1998; Inoue et al., 2002; Lin et al., 2000). Thus, the present study investigated the modulation of the short- and long-latency SEP components, using a forewarned reaction time task in which subjects were given a warning sound followed 2 s later by an electrical stimulus to the right median nerve at the wrist. They were instructed to respond by grasping with their hand when the electrical stimulus, which evoked the SEP, was presented. This task allowed us to examine the modulation of the early and subsequent cortical processing of the relevant somatosensory information, when the subject was required to perform the movement in response to it. We predicted the differential modulation of the short- and long-latency components even in this task. It is also possible that attention to the somatosensory stimulation modulates the SEP components, especially long-latency components (Desmedt and Robertson, 1977; Desmedt and Tomberg, 1983; Garcı`a-Larrea et al., 1995; Josiassen et al., 1982; Kida et al., 2004a,b; Michie et al., 1987). In addition to the movement task, therefore, a counting condition was carried out, in order to examine the attention effect.
2. Methods 2.1. Subjects Recordings were obtained from 9 healthy subjects (two women, 7 men), aged 24 – 30 years old. The left and right hands, and forearms were attached comfortably to the arm of the chair. Subjects gave informed consent. 2.2. Stimulus A pair of warning (S1) and imperative stimuli (S2) with a fixed interval of 2 s was presented. S1 was an auditory pure tone (70 dB SPL, 1000 Hz and 50 ms duration) presented through a loud speaker positioned in front of the subject’s nose at a distance of 1 m. S2 was an electric square wave constant current pulse (median nerve stimulation at the wrist, 0.2 ms duration, the intensity was sufficient to produce a slight but definite twitch of the thumb), and never produced any pain sensation in the subjects. S2 was omitted in 10% of trials, in order to prevent subjects from predicting the timing of contraction. The interval between successive auditory stimuli varied randomly between 4 and 7 s.
2.3. Condition Maximal voluntary contraction (MVC) was measured before the SEP measurement. In the rest condition, subjects relaxed and had no task, but their right hand was attached to a hand dynamometer as in the movement condition. In the movement condition, they were instructed to prepare to grip the hand dynamometer with a built-in force transducer on S1 without any muscle contraction, and to grip as fast and accurately as they could when the S2 was presented. Level of target force for grip movement (10% MVC) was displayed on an oscilloscope positioned in front of the subject’s nose at a distance of 1 m. In the counting condition, the subjects were instructed to count silently the number of the somatosensory stimuli. Each condition consisted of 3 blocks (one block: about 6 min). 2.4. Recordings and analysis The electroencephalography (5 – 1200 Hz) was recorded with Ag/AgCl electrodes from 9 scalp locations: Fz, Cz, Pz, F3, C3, P3, F4, C4, P4. All the scalp electrodes were referred to linked earlobes. Impedance was carefully balanced and maintained below 5 kV. The bandpass filter of 5– 1200 Hz virtually eliminates the CNV-like potential (Murase et al., 2000; Shimazu et al., 1999). The electrooculogram was recorded bipolarly from the right outer canthus and the suborbital region to monitor eye movements or blinks. The electromyography was recorded from extensor carpi radialis (ECR) muscle. The electromyography reaction time (EMGRT) was defined as the time from the imperative stimulus to sharp onset of EMG. The analysis period for SEPs was 250 ms, including a 50 ms pre-stimulus baseline. Trials exceeding ^ 60 mV were automatically excluded from averaging. In addition, trials with eyeblinks, eye movements and response errors were also excluded manually from averaging. Furthermore, trials with background EMG larger than ^ 50 mV within 80 ms after S2 were excluded (Murase et al., 2000). As a result, over 200 data could be averaged. The sampling rate of analoguedigital transformation was 5000 Hz. The peak amplitude of the SEPs was referenced to the peak of the preceding response, except for the P80 and N140 amplitudes. For the amplitude of each SEP component, an analysis of variance with repeated measures was performed for condition (rest, movement, and counting). Turkey’s multiple comparison was used for a post-hoc analysis. Statistical significance was set at P , 0:05:
3. Results Figs. 1 and 2 show the grand averaged SEP waveforms from 9 subjects. Each SEP component was labeled according to its latency, polarity, and electrode. The following components were consistently recorded in all
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P27 amplitudes at P3 were not significantly changed between conditions. In contrast to the attenuation of frontal N30 and central N60, the long-latency P80 (Cz and Pz) and N140 amplitudes (Fz and Cz) were significantly larger in the movement condition than in the rest condition. The P80 amplitude at Pz was significantly larger in the counting than in the rest condition, and showed a further increase from the counting condition to movement condition. The N140 amplitude was not significantly changed between the rest and counting conditions. Table 2 shows the mean and earliest EMGRT, and the P80 and N140 peak latencies. The P80 peak latency preceded the earliest EMGRT in all the subjects, whereas the N140 peak latency was later than the earliest EMGRT.
4. Discussion
Fig. 1. Grand averaged SEP waveforms (short-latency components). Black thick and thin lines represent the waveforms in the movement and rest conditions, respectively. Grey line represents that in the counting condition. Compared to the rest condition, N30 amplitude at Fz and F3, and N60 amplitude at C3 were attenuated in movement condition.
subjects, P14, N18, P20, N30 and N140 from Fz, P14, N18, P20, N30 and N140 from F3, P80 and N140 from Cz, P14, N18, P22, N30, P40 and N60 from C3, P80 from Pz, P14, and N20 and P27 from P3. Table 1 shows the amplitude values of SEP components. As a result of ANOVA, significant effects of condition were found for N30 and N140 at Fz, N30 at F3, P80 and N140 at Cz, N60 at C3, and P80 at Pz. Subcortical P14 amplitude at all the electrodes did not significantly change between conditions. The P20 amplitude at Fz and F3 did not significantly vary between the rest and movement conditions, whereas the N30 amplitude was significantly smaller in the movement condition than in the rest and count conditions. The amplitude of cortical components at C3 did not significantly vary between conditions, except for attenuated N60 in the movement condition. The N20 and
In the present study, the subcortical P14, central P22, frontal P20, parietal N20 and P27 were not significantly changed between the rest and movement conditions. In contrast, frontal N30 and central N60 were significantly smaller in amplitude in the movement than in the rest condition. No effect of counting on the short-latency components was found. These results indicate that the attenuation of the short-latency SEP components started before voluntary movement, and fit well with the previous results (Cheron and Borenstein, 1991; Cohen and Starr, 1987; Hazemann et al., 1975; Hoshiyama and Sheean, 1998; Jones et al., 1989; Murase et al., 2000; Shimazu et al., 1999; Wasaka et al., 2003). Shimazu et al. (1999) reported that frontal N30 and central N60 decreased in amplitude in the movement condition compared to the rest condition during the same task as used in the present study, whereas the frontal P22 and parietal N20 did not vary. They found no effect of counting on the early SEP components, suggesting that attention or concentration on somatosensory stimuli could not be responsible for gating. Murase et al. (2000) also reported an attenuation of frontal N30 without changes in frontal P22 and parietal N20 amplitudes in a similar task, whereas the attenuation was not observed when the subjects silently counted the number of somatosensory stimuli. Wasaka et al. (2003) reported that attenuation of the shortlatency SEF components started at least 500 ms before selfpaced voluntary movement, and was greater for the P30m than the N20m component. It has been reported that gating during movement occurs at several levels in the central nervous system. Ghez and Lenzi (1970) reported that the evoked response in the medial lemniscus of cats following stimulation of the superficial radial nerve was reduced in amplitude. In a subsequent study, it was shown that both presynaptic and postsynaptic inhibition occurred in the cuneate nucleus during voluntary contraction (Ghez and Pisa, 1972). The evoked potential at the somatosensory cortex in monkeys
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Fig. 2. Grand averaged SEP waveforms (long-latency components). Black thick and thin lines represent the waveforms in the movement and rest conditions, respectively. Grey line represents that in the counting condition. Compared to the rest condition, the P80 amplitude at Cz and Pz, and N140 amplitude at Fz and Cz were increased in the movement condition. The P80 amplitude was also larger in the counting than in the rest condition, and showed a further increase from the counting condition to the movement condition.
following forearm stimulation was decreased during active movement (Chapman et al. 1988; Jiang et al., 1990a), and the short-latency excitatory response in 89% of the neurons was also decreased (Jiang et al., 1991). In addition, intracortical microstimulation of the neurons in the motor cortex in the monkey produced a profound decrease in the magnitude of the short-latency component of the somatosensory evoked potentials (Jiang et al., 1990b), suggesting that the activities in the motor cortex could modulate the SEPs. The amplitude of P1 –N1 generated by neurons of the thalamic ventro-postero-lateral nucleus was decreased during movement in humans (Insola et al., 2004). In the present study, since the subcortical P14 and primary response N20 were not altered in the movement condition, the attenuation of the short-latency components may occur substantially at the cortical level. Previously, two mechanisms for the attenuation of SEPs during active movement have been considered: centrifugal
and centripetal gating mechanisms (Jones et al., 1989). The attenuation of short-latency SEPs is reported to be present when the stimulus precedes the onset of active movement (Cheron and Borenstein, 1991; Cohen and Starr, 1987; Jones et al., 1989), suggesting that there may be a centrifugal gating influence of motor centers on the sensory inputs. In contrast, the joint, cutaneous and muscle spindle afferents produce a significant interfering effect on SEP components. That is, the SEP is attenuated during both passive movement and continuous sensory stimulation (centripetal gating; Cheron and Borenstein, 1991; Jones, 1981; Kakigi et al., 1985). The attenuation of the frontal N30 component in the present study mainly resulted from the centrifugal mechanism, since it occurred before the onset of electromyography following active movement to the somatosensory response signal. If cortical motor neurons involved in active movement also take part in the generation of the cortical SEPs, those neurons involved in
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Table 1 Amplitudes of the SEP components (SE) Electrode
Component
Rest
Movement
Count
ANOVA
Fz
P14 N18 P20 N30 N140
1.56 (0.43) 21.60 (0.40) 1.58 (0.48) 23.99 (1.10) 24.35 (3.40)
1.56 (0.38) 21.57 (0.45) 1.57 (0.50) 23.22 (0.98)*/# 25.86 (3.48)*
1.54 (0.54) 21.68 (0.25) 1.39 (0.45) 23.94 (1.23) 24.49 (3.35)
n.s. n.s. n.s. P , 0:005 P , 0:05
F3
P14 N18 P20 N30 N140
1.81 (0.43) 21.54 (0.33) 1.75 (0.90) 24.14 (1.69) 23.48 (2.56)
1.60 (0.52) 21.50 (0.39) 1.52 (0.83) 23.19 (1.54) */# 24.92 (3.18)
1.64 (0.56) 21.69 (0.25) 1.71 (0.86) 24.10 (1.90) 23.91 (2.36)
n.s. n.s. n.s. P , 0.005 n.s.
Cz
P80 N140
4.27 (1.94) 22.85 (3.67)
6.41 (1.80)* 25.84 (4.15)*
4.56 (2.13) 22.83 (3.85)
P , 0:05 P , 0:05
C3
P14 N18 P22 N30 P40 N60
1.82 (0.66) 22.59 (0.99) 3.44 (0.80) 22.89 (1.75) 4.53 (0.99) 25.64 (1.56)
1.65 (0.54) 22.50 (0.83) 3.06 (0.96) 22.00 (1.23) 3.91 (1.06) 24.25 (1.25)*/#
1.67 (0.69) 22.64 (0.80) 3.43 (0.75) 22.95 (2.22) 4.35 (1.50) 25.04 (1.46)
n.s. n.s. n.s. n.s. n.s. P , 0:005
Pz P3
P80 P14 N20 P27
4.95 (1.14) 1.70 (0.69) 23.47 (1.31) 4.75 (0.93)
7.78 (1.63)*/# 1.51 (0.68) 23.13 (1.12) 4.21 (1.50)
6.33 (1.19)* 1.44 (0.64) 23.38 (1.03) 4.71 (0.96)
P , 0:005 n.s. n.s. n.s.
*P , 0:05 : vs. rest condition. #P , 0:05 : vs. counting condition.
movement would be unable to react to median nerve stimulation, resulting in smaller amplitude SEP. It is also possible that cortical motor neurons involved in producing the requested movement might suppress other cortical neurons involved in the generation of the SEP, a form of corticocortical inhibition (Cohen and Starr, 1987; Porter, 1981). In contrast to the centrifugal gating effect on the shortlatency components, long-latency P80 and N140 were enhanced in amplitude in the movement condition compared to the rest and the counting conditions. Because the P80 latency preceded the earliest EMG onset in all the subjects, the enhancement of the P80 amplitude was
substantially due to the centrifugal influence. Although the N140 latency did not precede the earliest EMG onset in all the subjects, the enhancement may be at least partly due to the centrifugal mechanism, based on the following reason. Peripheral afferents were generated about 10 ms after voluntary muscle activation (Vallbo, 1971). It takes about 20 ms for the peripheral afferents to reach the primary somatosensory cortex in humans, and about 70 and 120 ms to reach the generators of the P80 and the N140, respectively. It is conceivable that the N140 enhancement was due to the centrifugal effect unless the peripheral afferent impulse generated by voluntary muscle activation reached the generator before the N140
Table 2 Mean and fastest reaction times, and the P80 peak latency (Pz) in individual subjects Subject
Mean EMGRT
Earliest EMGRT
P80 peak latency
N140 peak latency
A B C D E F G H I
193.3 140.4 136.9 155.7 130.1 123.5 101.7 142.7 133.2
122.2 96.4 86.6 110.2 97.8 91.6 80.2 100.6 95.8
85.4 79.4 81.6 99.0 80.6 73.6 61.2 64.0 95.6
136.2 146.8 145.2 145.0 135.4 129.2 117.4 121.4 140.8
Mean
139.7
97.8
80.07
135.2667
24.9
12.5
12.72
SD
10.64331
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generation. Nakata et al. (2003) reported that the N140 amplitude increased during active finger movement, whereas they did not change during passive movement, suggesting that the centripetal mechanism could not be responsible for the N140 enhancement. In the S1 –S2 reaction time task (S1 – S2 interval: 4 s), Bo¨cker et al. (1993) also found that the P100 (our P80) -N140 increased in amplitude when an electrical stimulation was applied 500 ms before the visual reaction signal (S2). In contrast, the N70 – P100 decreased in amplitude, inconsistent with the present study. There was a difference in the timing of the electrical stimulation between the present and their experiments. In addition, we used an electrical stimulus, which evoked the SEPs, for stimulus detection (i.e. response signal). Hazemann et al. (1975) reported the enhanced amplitude of N130 (our N140) and the decreased amplitude of N65 before self-paced voluntary movement with the stimulated hand. In their study, the P95 (our P80) decreased in amplitude before and during self-paced movement, inconsistent with the present result. This discrepancy may result from the different modes of movement between the present and their studies. Cheron and Borenstein (1987) as well found an enhancement of N130 (our N140) in a selftriggered paradigm. Lee and White (1974) also observed an enhancement of N3 amplitude (our N140) when movements were performed by the stimulated hand. These previous findings and present studies raise the possibility that the N140 enhancement was due to the centrifugal influence. The enhancement of long-latency components may also result from the effect of attention to the stimulation (Desmedt and Robertson, 1977; Desmedt and Tomberg, 1983; Garcı`a-Larrea et al., 1995; Josiassen et al., 1982; Michie et al., 1987; Kida et al. 2004a,b). The present study found an attention effect on the P80 amplitude, with larger amplitude in the attention condition compared to the rest condition. Therefore, the P80 enhancement in the movement condition somewhat involved the attention effect. However, the P80 amplitude showed a further increase from the counting condition to the movement condition, suggesting an obvious centrifugal effect of voluntary movement. In contrast, no effect of attention on the N140 was found, inconsistent with the previous studies using the selective attention task. First, this controversy may result from the difference of stimulus interval between somatosensory stimuli in the present experiment (mean ISI ¼ 5.5 s). Because of the longer ISI, the N140 might have more time to recover than could increase with attention. However, Kida et al. (2004b) found a strong tendency of the N140 increase with attention, even when the ISI was relatively long (their deviant alone condition, mean ISI ¼ 4.0). Secondly, it may be related to the possibility that the N140 involves the endogenous negative potential related to selective attention such as a processing negativity (PN). It has sometimes been reported that the somatosensory PN did not appear at N1 peak, but between N1 and P2 (Michie, 1984; Michie et al., 1987). However, this was not the case at
the figure in the present study (such a negativity was not observed before and after the N140 peak). Thirdly, it was due to the task difference. The S1 – S2 simple reaction time task we used required only detection of the somatosensory stimulus, and therefore was easier (i.e. required smaller amounts of attention) than the selective attention task which requires discrimination between stimuli, accounting for the lack of enhancement of the N140 in the present study. The generator for the P80 and N140 has not yet been clarified. In intracranial recordings (Allison et al., 1989, 1992; Frot and Mauguie`re, 1999; Frot et al., 2001) and magnetoencephalography (MEG) studies (Hari et al., 1993; Mauguie`re et al., 1997; Hari and Forss, 1999; Kakigi et al., 2000), it has been shown that the SII area responded in the 70– 130 ms latency range to the somatosensory stimulation. Several investigators have reported interesting results in their MEG studies (Huttunen et al., 1996; Forss and Jousma¨ki, 1998; Inoue et al., 2002; Lin et al., 2000), and found that SII cortex activities in response to median nerve stimulation were enhanced during active movement (Huttunen et al., 1996; Forss and Jousma¨ki, 1998; Lin et al., 2000). This is in contrast to the attenuation of the SI activities during active movement (Kakigi et al., 1995). Enhanced SII activation during active movement may reflect tuning of the SII neurons towards relevant tactile impulses from the region of contracting muscles, which can help in monitoring and correcting the movements (Forss and Jousma¨ki, 1998; Hari and Forss, 1999). If the P80 component mainly consists of the SII activities, its enhancement in the present study may also be interpreted as evidence of the above-mentioned hypothesis. The P80 enhancement in the counting condition matches well with the MEG experiments where responses from the SII cortex increased with active attention (Hari and Forss, 1999; Mauguiere et al., 1997; Mima et al., 1998; Fujiwara et al., 2002). However, it should be noted that a N50 – P70 (N45 – P80) potential was recorded from the SI area and neighboring areas (Allison et al., 1989, 1992; Barba et al., 2004; Valeriani et al., 1997; ), and that a N70 – P100 potential was recorded from pre-SMA (Barba et al., 2001). In contrast to these activities which possibly contributed to scalp P80 potential, the frontal N140 was generated from the bilateral frontal lobes including the orbito-frontal cortex and lateral mesial cortex, and probably the supplementary motor cortex (Allison et al., 1989, 1992), or the activation of area 46 and complex reciprocal interaction between posterior and prefrontal cortex and subcortical structures (Desmedt and Tomberg, 1989; Kekoni et al., 1996), the activation of several areas in both hemispheres (Garcı`a-Larrea et al., 1995), the activation of the anterior cingulate gyrus (Waberski et al., 2002). In an MEG study, Forss et al. (1996) found activation of the mesial cortex at 120 – 160 ms in response to median nerve stimulation. Thus, different generator processes between the P80 and N140 may contribute to their different behaviors between the movement and counting conditions.
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In conclusion, the present study demonstrated the differential modulation of short- and long-latency components of SEPs in a forewarned reaction time task. The attenuation of the frontal N30 and central N60, and the enhancement of the P80 substantially resulted from the centrifugal effect, and they were relatively independent of attention effect (however, the P80 enhancement may involve the attention effect). Whether the N140 amplitude enhancement was due to the centrifugal or centripetal effects was unclear, but it was independent of the effect of attention to the stimulation in this paradigm. The differential modulation of the short- and long-latency components of the SEPs may reflect the different effects of voluntary movement on the early and subsequent cortical processing of relevant somatosensory information requiring behavioral response.
Acknowledgements This study was supported in part by the Nishihira/ Tsukuba Project of COE (Center of Excellence) from the Japan Ministry of Education, Culture, Sports, Science and Technology, and by the Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists.
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Differential modulation of the short- and long-latency somatosensory evoked potentials in a forewarned reaction time task Tetsuo Kidaa,*, Yoshiaki Nishihirab, Toshiaki Wasakaa, Yukie Sakajiric, Toshiki Tazoec a
Doctoral program in Health and Sports Sciences, University of Tsukuba, Tsukuba, Japan b Institute of Health and Sports Sciences, University of Tsukuba, Tsukuba, Japan c Master’s program in Health and Sports Sciences, University of Tsukuba, Tsukuba, Japan Accepted 22 April 2004 Available online 25 June 2004
Abstract Objective: We investigated modulation of the short- and long-latency somatosensory evoked potentials (SEPs) in a forewarned reaction time task. Methods: A pair of warning (auditory) and imperative stimuli (somatosensory) was presented with a 2 s interstimulus interval. In movement condition, subjects responded by grip movement with the ipsilateral hand to the somatosensory stimulation when the imperative stimulus was presented. In counting condition, they silently counted the number of imperative stimuli. The SEPs in response to the imperative stimuli were recorded. Results: Frontal N30 and central N60 amplitudes were significantly smaller in the movement than in the counting or rest conditions. None of the short-latency components differed between the counting and rest conditions. In contrast to the short-latency components, P80 was significantly larger in the counting than in the rest condition, and showed a further increase from the counting to the movement condition. The N140 amplitude was significantly larger in the movement than the rest condition, but was not changed between the counting and the rest conditions. Conclusions: The attenuation of the frontal N30 and central N60, and the enhancement of the P80 and possibly the N140 resulted from the centrifugal mechanism. The present findings may show the different effects of voluntary movement on the early and subsequent cortical processing of the relevant somatosensory information requiring a behavioral response. Significance: The present study demonstrated the differential modulation of short- and long-latency components of SEPs in a forewarned reaction time task. q 2004 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. Keywords: Somatosensory evoked potentials; Centrifugal gating; Attention; Voluntary movement
1. Introduction Relevant somatosensory information is influenced in various ways at different processing stages. This modulation of somatosensory information can be studied by somatosensory-evoked potentials (SEPs). Many studies have shown an attenuation of short-latency SEPs which occurs when a stimulus is delivered during active movement (Cheron and Borenstein, 1987, 1991, 1992; Cheron et al., 2000; Cohen and Starr, 1987; Nishihira et al., 1991; Rossini et al., 1996, 1999; Waberski et al., 1999; Valeriani et al., 1999). In these * Corresponding author. Fax: þ 81-29-853-2607. E-mail address: [email protected] (T. Kida).
previous studies, however, a somatosensory stimulus to evoke the SEPs was irrelevant to the subject’s movement task. There have been some attempts to examine the effects of voluntary movement or movement preparation on the SEPs in response to relevant stimulus. These studies found an attenuation of the SEPs when subjects responded to the somatosensory stimuli to evoke the SEPs (Asanuma et al., 2003; Murase et al., 2000; Shimazu et al., 1999). However, they did not show the data of long-latency SEP components (such P80 and N140 components). It has been reported that long-latency SEPs were attenuated (Jones, 1981; Rushton et al., 1981) or enhanced (Bo¨cker et al., 1993; Hazemann et al., 1975; Lee and White, 1974; Nakata et al., 2003) during voluntary movement.
1388-2457/$30.00 q 2004 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2004.04.017
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Recently, Nakata et al. (2003) reported the enhancement of the long-latency components during active movement. In addition to these SEP studies, magnetoencephalography (MEG) studies have shown that the short-latency SI activities were attenuated before and during voluntary movement (Kakigi et al., 1995; Wasaka et al., 2003), whereas the long-latency SII activities were enhanced (Huttunen et al., 1996; Forss and Jousmaki, 1998; Inoue et al., 2002; Lin et al., 2000). Thus, the present study investigated the modulation of the short- and long-latency SEP components, using a forewarned reaction time task in which subjects were given a warning sound followed 2 s later by an electrical stimulus to the right median nerve at the wrist. They were instructed to respond by grasping with their hand when the electrical stimulus, which evoked the SEP, was presented. This task allowed us to examine the modulation of the early and subsequent cortical processing of the relevant somatosensory information, when the subject was required to perform the movement in response to it. We predicted the differential modulation of the short- and long-latency components even in this task. It is also possible that attention to the somatosensory stimulation modulates the SEP components, especially long-latency components (Desmedt and Robertson, 1977; Desmedt and Tomberg, 1983; Garcı`a-Larrea et al., 1995; Josiassen et al., 1982; Kida et al., 2004a,b; Michie et al., 1987). In addition to the movement task, therefore, a counting condition was carried out, in order to examine the attention effect.
2. Methods 2.1. Subjects Recordings were obtained from 9 healthy subjects (two women, 7 men), aged 24 – 30 years old. The left and right hands, and forearms were attached comfortably to the arm of the chair. Subjects gave informed consent. 2.2. Stimulus A pair of warning (S1) and imperative stimuli (S2) with a fixed interval of 2 s was presented. S1 was an auditory pure tone (70 dB SPL, 1000 Hz and 50 ms duration) presented through a loud speaker positioned in front of the subject’s nose at a distance of 1 m. S2 was an electric square wave constant current pulse (median nerve stimulation at the wrist, 0.2 ms duration, the intensity was sufficient to produce a slight but definite twitch of the thumb), and never produced any pain sensation in the subjects. S2 was omitted in 10% of trials, in order to prevent subjects from predicting the timing of contraction. The interval between successive auditory stimuli varied randomly between 4 and 7 s.
2.3. Condition Maximal voluntary contraction (MVC) was measured before the SEP measurement. In the rest condition, subjects relaxed and had no task, but their right hand was attached to a hand dynamometer as in the movement condition. In the movement condition, they were instructed to prepare to grip the hand dynamometer with a built-in force transducer on S1 without any muscle contraction, and to grip as fast and accurately as they could when the S2 was presented. Level of target force for grip movement (10% MVC) was displayed on an oscilloscope positioned in front of the subject’s nose at a distance of 1 m. In the counting condition, the subjects were instructed to count silently the number of the somatosensory stimuli. Each condition consisted of 3 blocks (one block: about 6 min). 2.4. Recordings and analysis The electroencephalography (5 – 1200 Hz) was recorded with Ag/AgCl electrodes from 9 scalp locations: Fz, Cz, Pz, F3, C3, P3, F4, C4, P4. All the scalp electrodes were referred to linked earlobes. Impedance was carefully balanced and maintained below 5 kV. The bandpass filter of 5– 1200 Hz virtually eliminates the CNV-like potential (Murase et al., 2000; Shimazu et al., 1999). The electrooculogram was recorded bipolarly from the right outer canthus and the suborbital region to monitor eye movements or blinks. The electromyography was recorded from extensor carpi radialis (ECR) muscle. The electromyography reaction time (EMGRT) was defined as the time from the imperative stimulus to sharp onset of EMG. The analysis period for SEPs was 250 ms, including a 50 ms pre-stimulus baseline. Trials exceeding ^ 60 mV were automatically excluded from averaging. In addition, trials with eyeblinks, eye movements and response errors were also excluded manually from averaging. Furthermore, trials with background EMG larger than ^ 50 mV within 80 ms after S2 were excluded (Murase et al., 2000). As a result, over 200 data could be averaged. The sampling rate of analoguedigital transformation was 5000 Hz. The peak amplitude of the SEPs was referenced to the peak of the preceding response, except for the P80 and N140 amplitudes. For the amplitude of each SEP component, an analysis of variance with repeated measures was performed for condition (rest, movement, and counting). Turkey’s multiple comparison was used for a post-hoc analysis. Statistical significance was set at P , 0:05:
3. Results Figs. 1 and 2 show the grand averaged SEP waveforms from 9 subjects. Each SEP component was labeled according to its latency, polarity, and electrode. The following components were consistently recorded in all
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P27 amplitudes at P3 were not significantly changed between conditions. In contrast to the attenuation of frontal N30 and central N60, the long-latency P80 (Cz and Pz) and N140 amplitudes (Fz and Cz) were significantly larger in the movement condition than in the rest condition. The P80 amplitude at Pz was significantly larger in the counting than in the rest condition, and showed a further increase from the counting condition to movement condition. The N140 amplitude was not significantly changed between the rest and counting conditions. Table 2 shows the mean and earliest EMGRT, and the P80 and N140 peak latencies. The P80 peak latency preceded the earliest EMGRT in all the subjects, whereas the N140 peak latency was later than the earliest EMGRT.
4. Discussion
Fig. 1. Grand averaged SEP waveforms (short-latency components). Black thick and thin lines represent the waveforms in the movement and rest conditions, respectively. Grey line represents that in the counting condition. Compared to the rest condition, N30 amplitude at Fz and F3, and N60 amplitude at C3 were attenuated in movement condition.
subjects, P14, N18, P20, N30 and N140 from Fz, P14, N18, P20, N30 and N140 from F3, P80 and N140 from Cz, P14, N18, P22, N30, P40 and N60 from C3, P80 from Pz, P14, and N20 and P27 from P3. Table 1 shows the amplitude values of SEP components. As a result of ANOVA, significant effects of condition were found for N30 and N140 at Fz, N30 at F3, P80 and N140 at Cz, N60 at C3, and P80 at Pz. Subcortical P14 amplitude at all the electrodes did not significantly change between conditions. The P20 amplitude at Fz and F3 did not significantly vary between the rest and movement conditions, whereas the N30 amplitude was significantly smaller in the movement condition than in the rest and count conditions. The amplitude of cortical components at C3 did not significantly vary between conditions, except for attenuated N60 in the movement condition. The N20 and
In the present study, the subcortical P14, central P22, frontal P20, parietal N20 and P27 were not significantly changed between the rest and movement conditions. In contrast, frontal N30 and central N60 were significantly smaller in amplitude in the movement than in the rest condition. No effect of counting on the short-latency components was found. These results indicate that the attenuation of the short-latency SEP components started before voluntary movement, and fit well with the previous results (Cheron and Borenstein, 1991; Cohen and Starr, 1987; Hazemann et al., 1975; Hoshiyama and Sheean, 1998; Jones et al., 1989; Murase et al., 2000; Shimazu et al., 1999; Wasaka et al., 2003). Shimazu et al. (1999) reported that frontal N30 and central N60 decreased in amplitude in the movement condition compared to the rest condition during the same task as used in the present study, whereas the frontal P22 and parietal N20 did not vary. They found no effect of counting on the early SEP components, suggesting that attention or concentration on somatosensory stimuli could not be responsible for gating. Murase et al. (2000) also reported an attenuation of frontal N30 without changes in frontal P22 and parietal N20 amplitudes in a similar task, whereas the attenuation was not observed when the subjects silently counted the number of somatosensory stimuli. Wasaka et al. (2003) reported that attenuation of the shortlatency SEF components started at least 500 ms before selfpaced voluntary movement, and was greater for the P30m than the N20m component. It has been reported that gating during movement occurs at several levels in the central nervous system. Ghez and Lenzi (1970) reported that the evoked response in the medial lemniscus of cats following stimulation of the superficial radial nerve was reduced in amplitude. In a subsequent study, it was shown that both presynaptic and postsynaptic inhibition occurred in the cuneate nucleus during voluntary contraction (Ghez and Pisa, 1972). The evoked potential at the somatosensory cortex in monkeys
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Fig. 2. Grand averaged SEP waveforms (long-latency components). Black thick and thin lines represent the waveforms in the movement and rest conditions, respectively. Grey line represents that in the counting condition. Compared to the rest condition, the P80 amplitude at Cz and Pz, and N140 amplitude at Fz and Cz were increased in the movement condition. The P80 amplitude was also larger in the counting than in the rest condition, and showed a further increase from the counting condition to the movement condition.
following forearm stimulation was decreased during active movement (Chapman et al. 1988; Jiang et al., 1990a), and the short-latency excitatory response in 89% of the neurons was also decreased (Jiang et al., 1991). In addition, intracortical microstimulation of the neurons in the motor cortex in the monkey produced a profound decrease in the magnitude of the short-latency component of the somatosensory evoked potentials (Jiang et al., 1990b), suggesting that the activities in the motor cortex could modulate the SEPs. The amplitude of P1 –N1 generated by neurons of the thalamic ventro-postero-lateral nucleus was decreased during movement in humans (Insola et al., 2004). In the present study, since the subcortical P14 and primary response N20 were not altered in the movement condition, the attenuation of the short-latency components may occur substantially at the cortical level. Previously, two mechanisms for the attenuation of SEPs during active movement have been considered: centrifugal
and centripetal gating mechanisms (Jones et al., 1989). The attenuation of short-latency SEPs is reported to be present when the stimulus precedes the onset of active movement (Cheron and Borenstein, 1991; Cohen and Starr, 1987; Jones et al., 1989), suggesting that there may be a centrifugal gating influence of motor centers on the sensory inputs. In contrast, the joint, cutaneous and muscle spindle afferents produce a significant interfering effect on SEP components. That is, the SEP is attenuated during both passive movement and continuous sensory stimulation (centripetal gating; Cheron and Borenstein, 1991; Jones, 1981; Kakigi et al., 1985). The attenuation of the frontal N30 component in the present study mainly resulted from the centrifugal mechanism, since it occurred before the onset of electromyography following active movement to the somatosensory response signal. If cortical motor neurons involved in active movement also take part in the generation of the cortical SEPs, those neurons involved in
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Table 1 Amplitudes of the SEP components (SE) Electrode
Component
Rest
Movement
Count
ANOVA
Fz
P14 N18 P20 N30 N140
1.56 (0.43) 21.60 (0.40) 1.58 (0.48) 23.99 (1.10) 24.35 (3.40)
1.56 (0.38) 21.57 (0.45) 1.57 (0.50) 23.22 (0.98)*/# 25.86 (3.48)*
1.54 (0.54) 21.68 (0.25) 1.39 (0.45) 23.94 (1.23) 24.49 (3.35)
n.s. n.s. n.s. P , 0:005 P , 0:05
F3
P14 N18 P20 N30 N140
1.81 (0.43) 21.54 (0.33) 1.75 (0.90) 24.14 (1.69) 23.48 (2.56)
1.60 (0.52) 21.50 (0.39) 1.52 (0.83) 23.19 (1.54) */# 24.92 (3.18)
1.64 (0.56) 21.69 (0.25) 1.71 (0.86) 24.10 (1.90) 23.91 (2.36)
n.s. n.s. n.s. P , 0.005 n.s.
Cz
P80 N140
4.27 (1.94) 22.85 (3.67)
6.41 (1.80)* 25.84 (4.15)*
4.56 (2.13) 22.83 (3.85)
P , 0:05 P , 0:05
C3
P14 N18 P22 N30 P40 N60
1.82 (0.66) 22.59 (0.99) 3.44 (0.80) 22.89 (1.75) 4.53 (0.99) 25.64 (1.56)
1.65 (0.54) 22.50 (0.83) 3.06 (0.96) 22.00 (1.23) 3.91 (1.06) 24.25 (1.25)*/#
1.67 (0.69) 22.64 (0.80) 3.43 (0.75) 22.95 (2.22) 4.35 (1.50) 25.04 (1.46)
n.s. n.s. n.s. n.s. n.s. P , 0:005
Pz P3
P80 P14 N20 P27
4.95 (1.14) 1.70 (0.69) 23.47 (1.31) 4.75 (0.93)
7.78 (1.63)*/# 1.51 (0.68) 23.13 (1.12) 4.21 (1.50)
6.33 (1.19)* 1.44 (0.64) 23.38 (1.03) 4.71 (0.96)
P , 0:005 n.s. n.s. n.s.
*P , 0:05 : vs. rest condition. #P , 0:05 : vs. counting condition.
movement would be unable to react to median nerve stimulation, resulting in smaller amplitude SEP. It is also possible that cortical motor neurons involved in producing the requested movement might suppress other cortical neurons involved in the generation of the SEP, a form of corticocortical inhibition (Cohen and Starr, 1987; Porter, 1981). In contrast to the centrifugal gating effect on the shortlatency components, long-latency P80 and N140 were enhanced in amplitude in the movement condition compared to the rest and the counting conditions. Because the P80 latency preceded the earliest EMG onset in all the subjects, the enhancement of the P80 amplitude was
substantially due to the centrifugal influence. Although the N140 latency did not precede the earliest EMG onset in all the subjects, the enhancement may be at least partly due to the centrifugal mechanism, based on the following reason. Peripheral afferents were generated about 10 ms after voluntary muscle activation (Vallbo, 1971). It takes about 20 ms for the peripheral afferents to reach the primary somatosensory cortex in humans, and about 70 and 120 ms to reach the generators of the P80 and the N140, respectively. It is conceivable that the N140 enhancement was due to the centrifugal effect unless the peripheral afferent impulse generated by voluntary muscle activation reached the generator before the N140
Table 2 Mean and fastest reaction times, and the P80 peak latency (Pz) in individual subjects Subject
Mean EMGRT
Earliest EMGRT
P80 peak latency
N140 peak latency
A B C D E F G H I
193.3 140.4 136.9 155.7 130.1 123.5 101.7 142.7 133.2
122.2 96.4 86.6 110.2 97.8 91.6 80.2 100.6 95.8
85.4 79.4 81.6 99.0 80.6 73.6 61.2 64.0 95.6
136.2 146.8 145.2 145.0 135.4 129.2 117.4 121.4 140.8
Mean
139.7
97.8
80.07
135.2667
24.9
12.5
12.72
SD
10.64331
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generation. Nakata et al. (2003) reported that the N140 amplitude increased during active finger movement, whereas they did not change during passive movement, suggesting that the centripetal mechanism could not be responsible for the N140 enhancement. In the S1 –S2 reaction time task (S1 – S2 interval: 4 s), Bo¨cker et al. (1993) also found that the P100 (our P80) -N140 increased in amplitude when an electrical stimulation was applied 500 ms before the visual reaction signal (S2). In contrast, the N70 – P100 decreased in amplitude, inconsistent with the present study. There was a difference in the timing of the electrical stimulation between the present and their experiments. In addition, we used an electrical stimulus, which evoked the SEPs, for stimulus detection (i.e. response signal). Hazemann et al. (1975) reported the enhanced amplitude of N130 (our N140) and the decreased amplitude of N65 before self-paced voluntary movement with the stimulated hand. In their study, the P95 (our P80) decreased in amplitude before and during self-paced movement, inconsistent with the present result. This discrepancy may result from the different modes of movement between the present and their studies. Cheron and Borenstein (1987) as well found an enhancement of N130 (our N140) in a selftriggered paradigm. Lee and White (1974) also observed an enhancement of N3 amplitude (our N140) when movements were performed by the stimulated hand. These previous findings and present studies raise the possibility that the N140 enhancement was due to the centrifugal influence. The enhancement of long-latency components may also result from the effect of attention to the stimulation (Desmedt and Robertson, 1977; Desmedt and Tomberg, 1983; Garcı`a-Larrea et al., 1995; Josiassen et al., 1982; Michie et al., 1987; Kida et al. 2004a,b). The present study found an attention effect on the P80 amplitude, with larger amplitude in the attention condition compared to the rest condition. Therefore, the P80 enhancement in the movement condition somewhat involved the attention effect. However, the P80 amplitude showed a further increase from the counting condition to the movement condition, suggesting an obvious centrifugal effect of voluntary movement. In contrast, no effect of attention on the N140 was found, inconsistent with the previous studies using the selective attention task. First, this controversy may result from the difference of stimulus interval between somatosensory stimuli in the present experiment (mean ISI ¼ 5.5 s). Because of the longer ISI, the N140 might have more time to recover than could increase with attention. However, Kida et al. (2004b) found a strong tendency of the N140 increase with attention, even when the ISI was relatively long (their deviant alone condition, mean ISI ¼ 4.0). Secondly, it may be related to the possibility that the N140 involves the endogenous negative potential related to selective attention such as a processing negativity (PN). It has sometimes been reported that the somatosensory PN did not appear at N1 peak, but between N1 and P2 (Michie, 1984; Michie et al., 1987). However, this was not the case at
the figure in the present study (such a negativity was not observed before and after the N140 peak). Thirdly, it was due to the task difference. The S1 – S2 simple reaction time task we used required only detection of the somatosensory stimulus, and therefore was easier (i.e. required smaller amounts of attention) than the selective attention task which requires discrimination between stimuli, accounting for the lack of enhancement of the N140 in the present study. The generator for the P80 and N140 has not yet been clarified. In intracranial recordings (Allison et al., 1989, 1992; Frot and Mauguie`re, 1999; Frot et al., 2001) and magnetoencephalography (MEG) studies (Hari et al., 1993; Mauguie`re et al., 1997; Hari and Forss, 1999; Kakigi et al., 2000), it has been shown that the SII area responded in the 70– 130 ms latency range to the somatosensory stimulation. Several investigators have reported interesting results in their MEG studies (Huttunen et al., 1996; Forss and Jousma¨ki, 1998; Inoue et al., 2002; Lin et al., 2000), and found that SII cortex activities in response to median nerve stimulation were enhanced during active movement (Huttunen et al., 1996; Forss and Jousma¨ki, 1998; Lin et al., 2000). This is in contrast to the attenuation of the SI activities during active movement (Kakigi et al., 1995). Enhanced SII activation during active movement may reflect tuning of the SII neurons towards relevant tactile impulses from the region of contracting muscles, which can help in monitoring and correcting the movements (Forss and Jousma¨ki, 1998; Hari and Forss, 1999). If the P80 component mainly consists of the SII activities, its enhancement in the present study may also be interpreted as evidence of the above-mentioned hypothesis. The P80 enhancement in the counting condition matches well with the MEG experiments where responses from the SII cortex increased with active attention (Hari and Forss, 1999; Mauguiere et al., 1997; Mima et al., 1998; Fujiwara et al., 2002). However, it should be noted that a N50 – P70 (N45 – P80) potential was recorded from the SI area and neighboring areas (Allison et al., 1989, 1992; Barba et al., 2004; Valeriani et al., 1997; ), and that a N70 – P100 potential was recorded from pre-SMA (Barba et al., 2001). In contrast to these activities which possibly contributed to scalp P80 potential, the frontal N140 was generated from the bilateral frontal lobes including the orbito-frontal cortex and lateral mesial cortex, and probably the supplementary motor cortex (Allison et al., 1989, 1992), or the activation of area 46 and complex reciprocal interaction between posterior and prefrontal cortex and subcortical structures (Desmedt and Tomberg, 1989; Kekoni et al., 1996), the activation of several areas in both hemispheres (Garcı`a-Larrea et al., 1995), the activation of the anterior cingulate gyrus (Waberski et al., 2002). In an MEG study, Forss et al. (1996) found activation of the mesial cortex at 120 – 160 ms in response to median nerve stimulation. Thus, different generator processes between the P80 and N140 may contribute to their different behaviors between the movement and counting conditions.
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In conclusion, the present study demonstrated the differential modulation of short- and long-latency components of SEPs in a forewarned reaction time task. The attenuation of the frontal N30 and central N60, and the enhancement of the P80 substantially resulted from the centrifugal effect, and they were relatively independent of attention effect (however, the P80 enhancement may involve the attention effect). Whether the N140 amplitude enhancement was due to the centrifugal or centripetal effects was unclear, but it was independent of the effect of attention to the stimulation in this paradigm. The differential modulation of the short- and long-latency components of the SEPs may reflect the different effects of voluntary movement on the early and subsequent cortical processing of relevant somatosensory information requiring behavioral response.
Acknowledgements This study was supported in part by the Nishihira/ Tsukuba Project of COE (Center of Excellence) from the Japan Ministry of Education, Culture, Sports, Science and Technology, and by the Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists.
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