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Somatosensory N250 and P300 during discrimination tasks
International Journal of Psychophysiology 48 (2003) 275–283
Somatosensory N250 and P300 during discrimination tasks Tetsuo Kidaa,*, Yoshiaki Nishihirab, Arihiro Hattab, Toshiaki Wasakaa a
Doctoral Program in Health and Sport Sciences, University of Tsukuba, Tsukuba, Japan b Institute of Health and Sport Sciences, University of Tsukuba, Tsukuba, Japan
Received 10 September 2002; received in revised form 29 January 2003; accepted 4 February 2003
Abstract We investigated the event-related potentials (N250 and P300) during three kinds of somatosensory discrimination tasks (oddball task). Strong (standard: 90%) and weak (deviant: 10%) electrical stimuli were randomly delivered to the right median nerve at the wrist with a 500-ms constant interstimulus interval. In a passive situation, subjects read a self-selected book, ignoring all stimuli (ignore condition). One of the active situations was a mental counting task (count condition), and another required pressing a button to deviant stimuli as quickly as possible (motor response condition). The N250–P300 complex was elicited by deviant stimuli in the active-attended situations, but not found in the ignore condition. The N250 peak amplitude was unchanged between the count and motor response conditions whereas P300 changed. In addition, the N250 latency significantly correlated with the reaction time, but the P300 latency did not. These results indicate that the somatosensory N250 reflects an attentive process which is related to the temporal aspect of behavioral response. 䊚 2003 Elsevier Science B.V. All rights reserved. Keywords: Somatosensory; Attention; N250; P300; Active; Passive
1. Introduction In active oddball or discrimination situations, infrequent auditory deviant (target) stimuli elicit mismatch negativity (MMN), N2b, and late-positive components (P300) in human scalp-recorded event-related potentials (ERPs). In general, the MMN is elicited even in ignored situations such as reading a book, whereas the N2b–P300 complex is not elicited. Therefore, it has been considered that the N2b was attention-dependent and reflected *Corresponding author. Laboratory of Physiology, Tsukuba University School of Physical Education, Tennoudai 1-1-1, Tsukuba, Ibaraki, Japan. Tel.yfax: q81-29-853-2607. E-mail address: [email protected] (T. Kida).
¨¨ controlled processing in the attentive process (Naa¨ tanen, 1992). Analogous responses can also be measured to visual stimuli (Simson et al., 1977). Some researchers reported a strong relationship between the N2 and reaction time (RT) (Novak et al., 1990; Ritter et al., 1972, 1979). The N200–P300 complex to target tone in the active oddball situation has been recorded from the prefrontal cortex, caudate nucleus (Kropotov et al., 1995), anterior (Smith et al., 1990) or posterior (Halgren et al., 1995a) cingulate gyrus. Recently, Clarke et al. (1999) recorded intracranially N2-like components during a visual oddball task from the dorsolateral and ventrolateral prefrontal cortex, medial anteroventral temporal
0167-8760/03/$ - see front matter 䊚 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0167-8760(03)00021-7
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region, anterior and posterior hippocampal region, and parahippocampal region. These findings indicate that multiple cortical and subcortical regions are generators or activators of the scalp-recorded N2, as well as P300 (Baudena et al., 1995; Halgren et al., 1995b, 1998). It may be considered that the somatosensory N250 is analogous to auditory N2b or visual N2. Josiassen et al. (1982) reported somatosensory N230 and P400 deflections to target electric stimuli during a selective attention task. In their experiment, the N230 was not elicited by non-target stimuli. Ito et al. (1992) found N240 and P300 to rare non-target stimuli in addition to rare target stimuli. Kujala et al. (1995) recorded quite similar auditory N2b-P3 and somatosensory N250–P300 complexes in selective attention conditions where subjects attended to infrequent auditory or somatosensory deviants, ignoring the stimuli of the other modalities. Kekoni et al. (1996) did not find the N250–P300 complex elicited by vibratory deviant stimuli in the ignored oddball situation but did in the active situation. Thus, the somatosensory N250–P300 seems to be elicited by deviant stimuli in the active oddball situation as well as the auditory N2b–P3. However, the relationship between the N250 and the RT remains unknown. On the other hand, P300 is well known to be representative of the endogenous component. The functional significance of P300 is one of the controversial problems of the day, but the context updating theory seems to be most appropriate at the moment. That is, P300 is believed to index brain activity required in the maintenance of working memory when the mental model of the stimulus environment is updated (Donchin and Coles, 1988). The amplitude is also proportional to the amount of attentional resources devoted to a given task (Kramer and Strayer, 1988; Schubert et al., 1998; Wickens et al., 1983), whereas the latency is considered a measure of stimulus classification speed or stimulus evaluation time (Kutas et al., 1977) and is generally unrelated to response selection processes (McCarthy and Donchin, 1981; Pfefferbaum et al., 1983). The first purpose of the present study was to reassess the evidence that the somatosensory N250 reflects active target detection in attentive process.
For this purpose, we investigated the behavior of the N250 and P300 during the performance of three kinds of discrimination tasks (ignore, count, motor response) using somatosensory electrical stimuli. The second was to reveal the temporal relationship between the N250 and RT. 2. Materials and methods 2.1. Subjects Seven healthy right-handed subjects (ages 22– 27 years; six males, one female) participated in the experiment. They were sitting comfortably in an electrically shielded room. All the subjects reported no neurological or psychiatric problems and gave informed consent. 2.2. Stimuli The stimuli were delivered to the right median nerve at the wrist with a 500-ms constant interstimulus interval. Strong standard stimuli (frequent, 90%) were carefully adjusted to 1.15 times the strength of the twitch threshold and weak deviant (target) stimuli (infrequent, 10%) to 1.15 times the strength of the sensory threshold. These thresholds were first defined by the method of limits with ascending and descending levels of intensities (Desmedt and Tomberg, 1989). Two types of stimuli were presented in a pseudo-random order. It was ensured that the subjects could discriminate deviant stimuli from standard stimuli before the experiment. 2.3. Task All the subjects performed three tasks; ignore condition, count condition, motor response condition. Each condition consisted of a total 2000 stimuli, including 4 blocks (1 block 500 stimuli). In the ignore condition (passive), the subjects were asked to read a self-selected book, ignoring all stimuli. In the count condition (active), they kept a mental count of the number of deviant stimuli presented and were given feedback on the accuracy of their count at the end of each block in order to be encouraged to maintain a high level of accuracy.
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In the motor response condition (active), they were instructed to respond by pressing a button with the thumb of the right hand as fast as possible whenever a deviant stimulus was presented. The subject attended to the identical stimulus sequence in all the conditions. The order of conditions was counterbalanced across the subjects. The duration of an experiment was approximately 1 h excluding the recording preparation. In both the count and motor response conditions, the subjects were instructed to focus on a small fixation point positioned in front of them at a distance of approximately 2 m. 2.4. Recordings The electroencephalography (0.5–500 Hz) was recorded with AgyAgCl electrodes from 7 scalp locations: Fz, Cz, Pz, C3, C4, F39, P39 (F39 and C39 are 2 cm anterior, posterior to C3, respectively). All the scalp electrodes were referred to linked earlobes. The electro-oculogram was recorded bipolarly from the right outer canthus and the suborbital region to monitor eye movements or blinks. The analysis period of standard ERPs was 430 ms including a 50 ms prestimulus baseline. Deviant ERPs were analyzed for 550 ms including a 50 ms prestimulus baseline in order to avoid measurement mistakes due to longer latency of the P300. Peak amplitude of the P300 and N250 were obtained within this analysis period in all the subjects. Trials with eyeblinks, eye movements (rejection levels: "100 mV) and response errors were excluded from averaging. We rejected trials with slight artifacts in off-line analysis, in addition to automatic rejection. The sampling rate was 1 kHz. 2.5. Analysis First, in order to examine which conditions the P170, N250 and P300 responses were reliably observable in response to deviant (target) stimuli, three-factor analysis of variance with repeated measures (ANOVA) was performed (stimulus (2)=condition (3)=electrode (7)) for mean amplitude (P170: 130–180 ms, N250: 200–250 ms, P300: 280–380 ms). Second, the N250 and
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P300, which were determined from individual ERPs and their peak amplitudes, were measured from time windows of 190–270 and 280–480 ms, respectively. For the peak amplitude data, twofactor ANOVA with repeated measures was performed as factors for condition (count, motor response) and electrode (7 locations). The reported significances for the F values were those obtained after Greenhouse–Geisser correction when appropriate and then a correction coefficient epsilon was given. Statistical significance was set at P-0.05. The RT was measured between 150 and 500 ms after the stimulus onset every trial. The RT of trials excluded from averaging due to artifacts was not measured. Count accuracy was assessed by obtaining the absolute deviation of the subject’s target count from the correct target count for each of the four blocks, and then converting the total number of absolute errors to a percentage of the total correct count. 3. Results 3.1. Performance The percentage of errors in the count condition was 8.1%. Hit rate was 91.6% in the motor response condition, whereas there were few false alarms to standard stimuli. Mean RT across all the subjects was 364.16 ms. 3.2. ERPs Fig. 1 shows the grand-average waveforms of ERPs under each condition. The ERPs to standards remained unchanged between all the conditions. In the ignore condition, no distinct differences between standard and deviant ERPs were found. In contrast, in the count and motor response conditions, a positive–negative–positive deflection (we call P170, N250, P300, respectively) was clearly elicited by deviant stimuli. This deflection was obtained in all the subjects. However, since the P170 had a relatively low amplitude and a long duration, it was difficult to identify the peak from waveforms of some subjects. Therefore, the peak amplitude of P170 was not analyzed, but the mean amplitude of P170 was analyzed.
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Fig. 1. Grand-average ERPs in each condition. Thick and thin lines represent ERPs in response to deviant and standard stimuli, respectively.
3.2.1. Deviant vs. standard ERPs (mean amplitude) The difference between deviant and standard ERPs was assessed by mean amplitude value of each deflection. Table 1 shows mean amplitudes of the P170, N250 and P300. An interaction between three factors was significant with respect to P170 mean amplitude (Fs2.89, P-0.01). A main effect of stimulus was not obtained in the ignore condition, but P170 mean amplitude was larger for the deviant compared with the standard ERPs in both the count (Fs16.93, P-0.05) and motor response conditions (Fs6.46, P-0.05). The P170 showed a centro-parietal dominant distribution in both the count and motor response conditions. The N250 mean amplitude was larger for the deviant compared with the standard ERP overall (Fs13.76, P-0.05). Moreover, this stimulus effect differed between conditions among electrodes to yield a significant stimulus–condition– electrode interaction (Fs4.19, P-0.05). In the ignore condition, the N250 mean amplitude tended
to be larger for the deviant compared with the standard ERP, but was not significant (Fs4.55, Ps0.077). On the other hand, the N250 was larger significantly for the deviant compared with the standard ERP in both the count (Fs7.22, P0.05) and motor response conditions (Fs12.21, P-0.05). The P300 mean amplitude was larger for the deviant compared with the standard ERP overall (Fs15.74, P-0.01). Moreover, this stimulus effect differed between conditions among electrodes to yield a significant stimulus–condition– electrode interaction (Fs6.032, P-0.05), such that the motor response and count conditions produced a significant stimulus effect overall (count: Fs22.29, P-0.01; motor response: Fs 9.30, P-0.05) and especially at the centro-parietal electrodes (count: Fs7.75, P-0.01; motor response: Fs5.80, P-0.01), but the ignore condition showed no significant stimulus effect. In summary, P170–N250–P300 complex was elicited by deviant stimuli in active conditions, but not found in the ignore condition.
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Table 1 Mean amplitudes (mV"S.D.) of each deflection in all conditions Read Standard
Mental count Deviant
Standard
P170 Fz Cz Pz C3 C4 F39 P39
1.66"0.92 1.87"0.74 y0.17"0.52 1.45"0.72 0.50"0.37 1.40"0.92 0.71"1.54
1.61"1.33 1.98"1.58 0.43"0.86 0.69"1.06 0.79"0.61 1.08"1.23 0.20"0.92
1.66"1.01 1.94"1.07 y0.29"0.87 1.53"1.09 0.24"0.67 1.43"1.16 0.79"1.86
N250 Fz Cz Pz C3 C4 F39 P39
0.60"0.32 0.50"0.54 y0.11"0.86 0.58"0.50 0.02"0.56 0.51"0.17 0.36"0.85
y0.25"1.04 y0.39"1.48 y0.67"1.31 y0.08"0.73 y0.53"1.16 y0.12"0.67 y0.24"0.93
1.12"0.75 1.17"1.05 0.10"0.95 1.21"1.05 0.21"0.56 1.09"0.66 0.91"1.55
P300 Fz Cz Pz C3 C4 F39 P39
y0.15"0.48 y0.64"0.61 y0.47"0.41 y0.31"0.51 y0.34"0.46 y0.22"0.45 y0.31"0.51
0.06"0.86 y0.32"0.74 y0.22"0.65 y0.10"0.60 0.04"0.73 y0.07"0.84 y0.06"0.56
y0.44"0.37 y1.05"0.70 y0.89"0.59 y0.49"0.57 y0.75"0.39 y0.39"0.41 y0.51"0.68
Motor response Deviant 2.19"1.21 3.19"1.23*** 1.09"1.03*** 1.32"1.03 1.18"0.75*** 1.54"1.02 1.01"1.05 y0.88"2.04* y1.37"2.03* y0.25"1.17 y0.42"1.10* y1.42"1.79 y0.34"1.56* y0.37"0.83 2.50"1.57** 3.35"2.55*** 3.34"2.37*** 2.95"1.84*** 2.48"2.27** 2.59"1.44*** 3.27"2.34***
Standard 1.37"1.23 1.36"1.31 y0.66"0.76 1.14"1.36 0.08"0.72 1.08"1.40 0.23"1.89 1.27"0.74 1.43"1.16 0.36"0.90 1.18"0.97 0.51"0.60 1.06"0.61 0.85"1.46 y0.21"0.46 y0.85"0.88 y0.67"0.53 y0.51"0.68 y0.46"0.44 y0.31"0.57 y0.58"0.67
Deviant 1.76"1.48 2.29"2.09* 0.76"1.71** 1.06"1.13 0.75"0.94* 1.19"0.75 0.83"1.70* y0.32"1.40*** y1.39"1.75** y0.14"1.58 y0.09"0.99** y1.09"1.93 0.28"1.23* y0.45"1.07 1.40"1.66* 2.44"3.32* 3.20"3.16* 2.21"2.39* 2.24"2.45* 1.61"1.62* 2.86"3.20*
*P-0.05, **P-0.01, ***P-0.005 (standard vs. deviant).
3.2.2. Peak amplitude and latency of N250 and P300 There were no significant effects on N250 and P300 peak latencies. Table 2 shows peak amplitudes of the P170, N250 and P300. The N250 peak amplitude variation between the different electrodes was significant (Fs6.01, P-0.01, ´s 0.415). Post hoc multiple comparisons revealed a central-dominant distribution of the N250 in both active-attended tasks (Cz)Pz, Cz)C3, Cz)F39, Cz)P39, P-0.05). A main effect of condition, and an interaction between condition and electrode were not significant. For the P300 peak amplitude, main effects of both electrode (Fs6.22, P-0.001) and condition (Fs6.11, P-0.05) were significant. An interaction between electrode and condition was also significant (Fs3.60, P-0.01). The P300 amplitudes were larger in the count condition at all the
electrodes compared with the motor response condition, and the difference reached significance at Fz (ts5.33, P-0.05), F39 (ts5.41, P-0.05) and C3 (ts2.58, P-0.05). To assess possible scalp distribution differences between conditions, P300 amplitudes were normalized using the vector method (McCarthy and Wood, 1985; Katayama and Polich, 1996; Mertens and Polich, 1997). Two-factor ANOVA of P300 peak amplitude normalized by this procedure remained stable to produce a significant interaction between condition and electrode (Fs4.23, P0.005). Unlike before the normalization, however, post hoc t-test indicated that the P300 peak amplitude was larger only at Fz during the count compared with the motor response condition (ts 2.86, P-0.05). Therefore, scalp distribution differences among the conditions may be due to frontal activities, possibly anterior P3.
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Table 2 N250 and P300 peak amplitudes (mV"S.D.) in the count and motor response conditions
with the RT (rs0.93, P-0.05), but the P300 latency did not (rs0.64, n.s.).
Mental count
Motor response
4. Discussion
N250 Fz Cz Pz C3 C4 F39 P39
y2.90"1.48 y3.96"1.43 y2.31"0.93 y2.36"1.02 y3.24"1.13 y2.30"1.42 y2.31"0.86
y2.27"1.27 y4.18"1.43 y2.33"0.99 y2.09"0.87 y2.95"1.35 y1.52"1.13 y2.61"0.85
P300 Fz Cz Pz C3 C4 F39 P39
In the present study, we found that (1) the P170–N250–P300 complex was elicited by deviant stimuli in active-attended conditions, but not found in the ignore condition, (2) the N250 latency highly correlated with the RT and (3) the P300 peak amplitude changed between the count and motor response conditions.
4.58"1.24 5.92"1.98 5.83"2.18 5.10"1.59 4.50"1.69 4.57"1.37 5.68"1.94
*
3.19"1.54* 5.00"3.07 5.69"2.70 4.29"1.93* 4.30"2.22 3.43"1.61* 5.18"2.62
P-0.05 (count vs. motor response).
3.2.3. Relationship between ERP peak latency and reaction time Fig. 2 shows the RT and the peak latency of N250 (Cz) and P300 (Pz). The N250 peak latency was earlier than the RT in all the subjects, while the P300 peak latency tended to be later than the RT in most cases. The N250 peak latency in the motor response condition significantly correlated
4.1. N250 The N250 was not apparent in the ignore condition, whereas it was largely elicited by deviant stimuli in active-attended conditions. This result indicates that the N250 reflects active target detection in an attentive process. Kekoni et al. (1996) reported a similar result using vibratory deviant stimuli, and, therefore, suggested that the N250 might reflect the conscious target detection. Furthermore, we found the N250 in response to deviant stimuli in both the count and motor response conditions. Most of the other previous studies have also shown that the N250 was elicited by rare target stimuli (Josiassen et al., 1982; Kujala et al., 1995). However, Ito et al. (1992) and
Fig. 2. The RT and the peak latency of N250 and P300 in the motor response condition. A circle and triangle represent the data of one subject.
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Kekoni et al. (1997) reported the N250 in response to rare non-target stimuli. This may be interpreted by attentional leaking (Kekoni et al., 1996, 1997). Consistent with this idea, Kekoni et al. (1997) reported that small N250 occurred because highfrequency vibratory deviant stimuli captured the subject’s attention in an ignore condition (reading condition). Also, in Ito’s experiment non-target N250 was followed by a small P300 and slow wave, which might index involuntary shifts of attention (Kekoni et al., 1996). It may be interpreted that the attentional capturing toward deviant stimuli did not occur in the ignore condition. The fronto-central distribution of the N250 was of the same shape as the distributions of the ¨¨ ¨ auditory N2b in previous studies (Naatanen, 1992). This distribution matches well with human intracranial recordings in which the N200–P300 complex was observed from the human cingulate gyrus or frontal cortex (Baudena et al., 1995; Clarke et al., 1999; Kropotov et al., 1995; Smith et al., 1990). Kekoni et al. (1996) reported that the N250 was broadly distributed and maximal at a contralateral frontal electrode. In the present experiment, the N250 was maximal at the central electrode but we did not record at the lateral frontal site. Further investigation is needed in order to reveal the distribution of N250. Interestingly, the N250 peak latency highly correlated with the RT, whereas the P300 latency did not significantly. Furthermore, the N250 peak latency was earlier than the RT in all the subjects, while the P300 peak latency tended to be later in most cases. This result shows that the N250 is closely related to the RT and was in agreement with that of the other modalities. Unlike the P300, the auditory or visual N2 is elicited at earlier latency than the RT (Ritter et al., 1972; Renault et al., 1982). Furthermore, the N2 latency shows a strong relationship to the RT (Novak et al., 1990; Ritter et al., 1972, 1979). In contrast, although the P300 latency often correlates with the RT, sometimes it precedes the RT and sometimes it is later than the RT (Donchin and Coles, 1988). Therefore, N2 can more directly measure the absolute timing of certain processes (Ritter et al., 1979), while P300 latency reflects the stimulus evaluation time (Kutas et al., 1977; Verleger,
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1997) or post-decision closure (Desmedt, 1980). The present results are consistent with the above hypothesis of P300 latency, and show that the N250 may reflect an attentive process which controls behavioral responses in somatosensory discrimination tasks. 4.2. P300 Theoretically, P300 is an endogenous component which accompanies the context updating within the working memory stores (Donchin and Coles, 1988), and its amplitude is proportional to the amount of attentional resources devoted to a given task (Kramer and Strayer, 1988; Schubert et al., 1998; Wickens et al., 1983). One interpretation of the P300 modulation between conditions is due to working memory load. Deviant stimuli in the count condition require updates of the number within the working memory stores but not in the motor response condition. Therefore, working memory load was higher in the count compared to the motor response condition, resulting in enhanced amplitude of the P300. This assumption is consistent with the idea that the frontal association area plays an essential role in working memory, because the increase of the P300 amplitude was more remarkable at the frontal site. Furthermore, such a high working memory load would force subjects to allocate more attentional resources to a given task. Therefore, this interpretation is also in agreement with the hypothesis that the P300 amplitude reflects the amount of attentional resources. Second, it may be due to the specific allocation of attentional resources to the stimulus processing. Because subjects were asked to press a button as quickly as possible in the motor response condition, attentional resource would be allocated to not only the stimulus sequence but also the movement, whereas they only had to allocate to the stimulus sequence in the count condition. The third explanation is that the P300 modulation is based on the P3 related to the attentional orienting toward relevant stimuli. The P300 amplitude decreased especially at the frontal site in the motor response condition, suggesting that the orienting response toward relevant stimuli was suppressed by a button-pressing response.
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In the previous studies, the difference of P300 amplitude between the motor response and count tasks seems to be controversial. Johnson (1986) reported that the P300 amplitude appeared larger for a button-pressing response than for a count response. In contrast, Polich (1987) reported that the P300 amplitude was larger for a count response than for a button-pressing response. Barrett et al. (1987) also reported that the P300 amplitude was larger for a count response compared to a buttonpressing response, but this was caused by overlapping of motor-related potentials because the P300 amplitude was smaller at Cz and C3 for a buttonpressing response compared to a count response when subjects responded by pressing a button with the right index finger. Moreover, Starr et al. (1995, 1997) reported no difference in the P300 amplitude between button-pressing and silent-counting. Mertens and Polich (1997) did not seem to mention the difference of P300 amplitudes between response conditions. Although it is difficult to resolve these contradictions, at least present and previous results indicate that the P300 amplitude is sensitive to a given task. In conclusion, the present study indicated that the somatosensory N250 might reflect active target detection in an attentive process. The changes in the P300 amplitude between the mental count and motor response conditions may be related to variations in working memory load. References Baudena, P., Halgren, E., Heit, G., Clarke, J.M., 1995. Intracerebral potentials to rare target and distractor auditory and visual stimuli. III. Frontal cortex. Electroen. Clin. Neuro. 94, 251–264. Barrett, G., Neshige, R., Shibasaki, H., 1987. Human auditory and somatosensory event-related potentials: effects of response condition and age. Electroen. Clin. Neuro. 66, 409–419. Clarke, J.M., Halgren, E., Chauvel, P., 1999. Intracranial ERPs in humans during a lateralized visual oddball task; II. Temporal, parietal, and frontal recordings. Clin. Neurophysiol. 110, 1226–1244. Desmedt, J.E., 1980. P300 in serial tasks: an essential postdecision closure mechanism. Prog. Brain Res. 54, 682–686. Desmedt, J.E., Tomberg, C., 1989. Mapping early somatosensory evoked potentials in selective attention: critical evaluation of control conditions used for titrating by difference
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Somatosensory N250 and P300 during discrimination tasks Tetsuo Kidaa,*, Yoshiaki Nishihirab, Arihiro Hattab, Toshiaki Wasakaa a
Doctoral Program in Health and Sport Sciences, University of Tsukuba, Tsukuba, Japan b Institute of Health and Sport Sciences, University of Tsukuba, Tsukuba, Japan
Received 10 September 2002; received in revised form 29 January 2003; accepted 4 February 2003
Abstract We investigated the event-related potentials (N250 and P300) during three kinds of somatosensory discrimination tasks (oddball task). Strong (standard: 90%) and weak (deviant: 10%) electrical stimuli were randomly delivered to the right median nerve at the wrist with a 500-ms constant interstimulus interval. In a passive situation, subjects read a self-selected book, ignoring all stimuli (ignore condition). One of the active situations was a mental counting task (count condition), and another required pressing a button to deviant stimuli as quickly as possible (motor response condition). The N250–P300 complex was elicited by deviant stimuli in the active-attended situations, but not found in the ignore condition. The N250 peak amplitude was unchanged between the count and motor response conditions whereas P300 changed. In addition, the N250 latency significantly correlated with the reaction time, but the P300 latency did not. These results indicate that the somatosensory N250 reflects an attentive process which is related to the temporal aspect of behavioral response. 䊚 2003 Elsevier Science B.V. All rights reserved. Keywords: Somatosensory; Attention; N250; P300; Active; Passive
1. Introduction In active oddball or discrimination situations, infrequent auditory deviant (target) stimuli elicit mismatch negativity (MMN), N2b, and late-positive components (P300) in human scalp-recorded event-related potentials (ERPs). In general, the MMN is elicited even in ignored situations such as reading a book, whereas the N2b–P300 complex is not elicited. Therefore, it has been considered that the N2b was attention-dependent and reflected *Corresponding author. Laboratory of Physiology, Tsukuba University School of Physical Education, Tennoudai 1-1-1, Tsukuba, Ibaraki, Japan. Tel.yfax: q81-29-853-2607. E-mail address: [email protected] (T. Kida).
¨¨ controlled processing in the attentive process (Naa¨ tanen, 1992). Analogous responses can also be measured to visual stimuli (Simson et al., 1977). Some researchers reported a strong relationship between the N2 and reaction time (RT) (Novak et al., 1990; Ritter et al., 1972, 1979). The N200–P300 complex to target tone in the active oddball situation has been recorded from the prefrontal cortex, caudate nucleus (Kropotov et al., 1995), anterior (Smith et al., 1990) or posterior (Halgren et al., 1995a) cingulate gyrus. Recently, Clarke et al. (1999) recorded intracranially N2-like components during a visual oddball task from the dorsolateral and ventrolateral prefrontal cortex, medial anteroventral temporal
0167-8760/03/$ - see front matter 䊚 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0167-8760(03)00021-7
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region, anterior and posterior hippocampal region, and parahippocampal region. These findings indicate that multiple cortical and subcortical regions are generators or activators of the scalp-recorded N2, as well as P300 (Baudena et al., 1995; Halgren et al., 1995b, 1998). It may be considered that the somatosensory N250 is analogous to auditory N2b or visual N2. Josiassen et al. (1982) reported somatosensory N230 and P400 deflections to target electric stimuli during a selective attention task. In their experiment, the N230 was not elicited by non-target stimuli. Ito et al. (1992) found N240 and P300 to rare non-target stimuli in addition to rare target stimuli. Kujala et al. (1995) recorded quite similar auditory N2b-P3 and somatosensory N250–P300 complexes in selective attention conditions where subjects attended to infrequent auditory or somatosensory deviants, ignoring the stimuli of the other modalities. Kekoni et al. (1996) did not find the N250–P300 complex elicited by vibratory deviant stimuli in the ignored oddball situation but did in the active situation. Thus, the somatosensory N250–P300 seems to be elicited by deviant stimuli in the active oddball situation as well as the auditory N2b–P3. However, the relationship between the N250 and the RT remains unknown. On the other hand, P300 is well known to be representative of the endogenous component. The functional significance of P300 is one of the controversial problems of the day, but the context updating theory seems to be most appropriate at the moment. That is, P300 is believed to index brain activity required in the maintenance of working memory when the mental model of the stimulus environment is updated (Donchin and Coles, 1988). The amplitude is also proportional to the amount of attentional resources devoted to a given task (Kramer and Strayer, 1988; Schubert et al., 1998; Wickens et al., 1983), whereas the latency is considered a measure of stimulus classification speed or stimulus evaluation time (Kutas et al., 1977) and is generally unrelated to response selection processes (McCarthy and Donchin, 1981; Pfefferbaum et al., 1983). The first purpose of the present study was to reassess the evidence that the somatosensory N250 reflects active target detection in attentive process.
For this purpose, we investigated the behavior of the N250 and P300 during the performance of three kinds of discrimination tasks (ignore, count, motor response) using somatosensory electrical stimuli. The second was to reveal the temporal relationship between the N250 and RT. 2. Materials and methods 2.1. Subjects Seven healthy right-handed subjects (ages 22– 27 years; six males, one female) participated in the experiment. They were sitting comfortably in an electrically shielded room. All the subjects reported no neurological or psychiatric problems and gave informed consent. 2.2. Stimuli The stimuli were delivered to the right median nerve at the wrist with a 500-ms constant interstimulus interval. Strong standard stimuli (frequent, 90%) were carefully adjusted to 1.15 times the strength of the twitch threshold and weak deviant (target) stimuli (infrequent, 10%) to 1.15 times the strength of the sensory threshold. These thresholds were first defined by the method of limits with ascending and descending levels of intensities (Desmedt and Tomberg, 1989). Two types of stimuli were presented in a pseudo-random order. It was ensured that the subjects could discriminate deviant stimuli from standard stimuli before the experiment. 2.3. Task All the subjects performed three tasks; ignore condition, count condition, motor response condition. Each condition consisted of a total 2000 stimuli, including 4 blocks (1 block 500 stimuli). In the ignore condition (passive), the subjects were asked to read a self-selected book, ignoring all stimuli. In the count condition (active), they kept a mental count of the number of deviant stimuli presented and were given feedback on the accuracy of their count at the end of each block in order to be encouraged to maintain a high level of accuracy.
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In the motor response condition (active), they were instructed to respond by pressing a button with the thumb of the right hand as fast as possible whenever a deviant stimulus was presented. The subject attended to the identical stimulus sequence in all the conditions. The order of conditions was counterbalanced across the subjects. The duration of an experiment was approximately 1 h excluding the recording preparation. In both the count and motor response conditions, the subjects were instructed to focus on a small fixation point positioned in front of them at a distance of approximately 2 m. 2.4. Recordings The electroencephalography (0.5–500 Hz) was recorded with AgyAgCl electrodes from 7 scalp locations: Fz, Cz, Pz, C3, C4, F39, P39 (F39 and C39 are 2 cm anterior, posterior to C3, respectively). All the scalp electrodes were referred to linked earlobes. The electro-oculogram was recorded bipolarly from the right outer canthus and the suborbital region to monitor eye movements or blinks. The analysis period of standard ERPs was 430 ms including a 50 ms prestimulus baseline. Deviant ERPs were analyzed for 550 ms including a 50 ms prestimulus baseline in order to avoid measurement mistakes due to longer latency of the P300. Peak amplitude of the P300 and N250 were obtained within this analysis period in all the subjects. Trials with eyeblinks, eye movements (rejection levels: "100 mV) and response errors were excluded from averaging. We rejected trials with slight artifacts in off-line analysis, in addition to automatic rejection. The sampling rate was 1 kHz. 2.5. Analysis First, in order to examine which conditions the P170, N250 and P300 responses were reliably observable in response to deviant (target) stimuli, three-factor analysis of variance with repeated measures (ANOVA) was performed (stimulus (2)=condition (3)=electrode (7)) for mean amplitude (P170: 130–180 ms, N250: 200–250 ms, P300: 280–380 ms). Second, the N250 and
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P300, which were determined from individual ERPs and their peak amplitudes, were measured from time windows of 190–270 and 280–480 ms, respectively. For the peak amplitude data, twofactor ANOVA with repeated measures was performed as factors for condition (count, motor response) and electrode (7 locations). The reported significances for the F values were those obtained after Greenhouse–Geisser correction when appropriate and then a correction coefficient epsilon was given. Statistical significance was set at P-0.05. The RT was measured between 150 and 500 ms after the stimulus onset every trial. The RT of trials excluded from averaging due to artifacts was not measured. Count accuracy was assessed by obtaining the absolute deviation of the subject’s target count from the correct target count for each of the four blocks, and then converting the total number of absolute errors to a percentage of the total correct count. 3. Results 3.1. Performance The percentage of errors in the count condition was 8.1%. Hit rate was 91.6% in the motor response condition, whereas there were few false alarms to standard stimuli. Mean RT across all the subjects was 364.16 ms. 3.2. ERPs Fig. 1 shows the grand-average waveforms of ERPs under each condition. The ERPs to standards remained unchanged between all the conditions. In the ignore condition, no distinct differences between standard and deviant ERPs were found. In contrast, in the count and motor response conditions, a positive–negative–positive deflection (we call P170, N250, P300, respectively) was clearly elicited by deviant stimuli. This deflection was obtained in all the subjects. However, since the P170 had a relatively low amplitude and a long duration, it was difficult to identify the peak from waveforms of some subjects. Therefore, the peak amplitude of P170 was not analyzed, but the mean amplitude of P170 was analyzed.
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Fig. 1. Grand-average ERPs in each condition. Thick and thin lines represent ERPs in response to deviant and standard stimuli, respectively.
3.2.1. Deviant vs. standard ERPs (mean amplitude) The difference between deviant and standard ERPs was assessed by mean amplitude value of each deflection. Table 1 shows mean amplitudes of the P170, N250 and P300. An interaction between three factors was significant with respect to P170 mean amplitude (Fs2.89, P-0.01). A main effect of stimulus was not obtained in the ignore condition, but P170 mean amplitude was larger for the deviant compared with the standard ERPs in both the count (Fs16.93, P-0.05) and motor response conditions (Fs6.46, P-0.05). The P170 showed a centro-parietal dominant distribution in both the count and motor response conditions. The N250 mean amplitude was larger for the deviant compared with the standard ERP overall (Fs13.76, P-0.05). Moreover, this stimulus effect differed between conditions among electrodes to yield a significant stimulus–condition– electrode interaction (Fs4.19, P-0.05). In the ignore condition, the N250 mean amplitude tended
to be larger for the deviant compared with the standard ERP, but was not significant (Fs4.55, Ps0.077). On the other hand, the N250 was larger significantly for the deviant compared with the standard ERP in both the count (Fs7.22, P0.05) and motor response conditions (Fs12.21, P-0.05). The P300 mean amplitude was larger for the deviant compared with the standard ERP overall (Fs15.74, P-0.01). Moreover, this stimulus effect differed between conditions among electrodes to yield a significant stimulus–condition– electrode interaction (Fs6.032, P-0.05), such that the motor response and count conditions produced a significant stimulus effect overall (count: Fs22.29, P-0.01; motor response: Fs 9.30, P-0.05) and especially at the centro-parietal electrodes (count: Fs7.75, P-0.01; motor response: Fs5.80, P-0.01), but the ignore condition showed no significant stimulus effect. In summary, P170–N250–P300 complex was elicited by deviant stimuli in active conditions, but not found in the ignore condition.
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Table 1 Mean amplitudes (mV"S.D.) of each deflection in all conditions Read Standard
Mental count Deviant
Standard
P170 Fz Cz Pz C3 C4 F39 P39
1.66"0.92 1.87"0.74 y0.17"0.52 1.45"0.72 0.50"0.37 1.40"0.92 0.71"1.54
1.61"1.33 1.98"1.58 0.43"0.86 0.69"1.06 0.79"0.61 1.08"1.23 0.20"0.92
1.66"1.01 1.94"1.07 y0.29"0.87 1.53"1.09 0.24"0.67 1.43"1.16 0.79"1.86
N250 Fz Cz Pz C3 C4 F39 P39
0.60"0.32 0.50"0.54 y0.11"0.86 0.58"0.50 0.02"0.56 0.51"0.17 0.36"0.85
y0.25"1.04 y0.39"1.48 y0.67"1.31 y0.08"0.73 y0.53"1.16 y0.12"0.67 y0.24"0.93
1.12"0.75 1.17"1.05 0.10"0.95 1.21"1.05 0.21"0.56 1.09"0.66 0.91"1.55
P300 Fz Cz Pz C3 C4 F39 P39
y0.15"0.48 y0.64"0.61 y0.47"0.41 y0.31"0.51 y0.34"0.46 y0.22"0.45 y0.31"0.51
0.06"0.86 y0.32"0.74 y0.22"0.65 y0.10"0.60 0.04"0.73 y0.07"0.84 y0.06"0.56
y0.44"0.37 y1.05"0.70 y0.89"0.59 y0.49"0.57 y0.75"0.39 y0.39"0.41 y0.51"0.68
Motor response Deviant 2.19"1.21 3.19"1.23*** 1.09"1.03*** 1.32"1.03 1.18"0.75*** 1.54"1.02 1.01"1.05 y0.88"2.04* y1.37"2.03* y0.25"1.17 y0.42"1.10* y1.42"1.79 y0.34"1.56* y0.37"0.83 2.50"1.57** 3.35"2.55*** 3.34"2.37*** 2.95"1.84*** 2.48"2.27** 2.59"1.44*** 3.27"2.34***
Standard 1.37"1.23 1.36"1.31 y0.66"0.76 1.14"1.36 0.08"0.72 1.08"1.40 0.23"1.89 1.27"0.74 1.43"1.16 0.36"0.90 1.18"0.97 0.51"0.60 1.06"0.61 0.85"1.46 y0.21"0.46 y0.85"0.88 y0.67"0.53 y0.51"0.68 y0.46"0.44 y0.31"0.57 y0.58"0.67
Deviant 1.76"1.48 2.29"2.09* 0.76"1.71** 1.06"1.13 0.75"0.94* 1.19"0.75 0.83"1.70* y0.32"1.40*** y1.39"1.75** y0.14"1.58 y0.09"0.99** y1.09"1.93 0.28"1.23* y0.45"1.07 1.40"1.66* 2.44"3.32* 3.20"3.16* 2.21"2.39* 2.24"2.45* 1.61"1.62* 2.86"3.20*
*P-0.05, **P-0.01, ***P-0.005 (standard vs. deviant).
3.2.2. Peak amplitude and latency of N250 and P300 There were no significant effects on N250 and P300 peak latencies. Table 2 shows peak amplitudes of the P170, N250 and P300. The N250 peak amplitude variation between the different electrodes was significant (Fs6.01, P-0.01, ´s 0.415). Post hoc multiple comparisons revealed a central-dominant distribution of the N250 in both active-attended tasks (Cz)Pz, Cz)C3, Cz)F39, Cz)P39, P-0.05). A main effect of condition, and an interaction between condition and electrode were not significant. For the P300 peak amplitude, main effects of both electrode (Fs6.22, P-0.001) and condition (Fs6.11, P-0.05) were significant. An interaction between electrode and condition was also significant (Fs3.60, P-0.01). The P300 amplitudes were larger in the count condition at all the
electrodes compared with the motor response condition, and the difference reached significance at Fz (ts5.33, P-0.05), F39 (ts5.41, P-0.05) and C3 (ts2.58, P-0.05). To assess possible scalp distribution differences between conditions, P300 amplitudes were normalized using the vector method (McCarthy and Wood, 1985; Katayama and Polich, 1996; Mertens and Polich, 1997). Two-factor ANOVA of P300 peak amplitude normalized by this procedure remained stable to produce a significant interaction between condition and electrode (Fs4.23, P0.005). Unlike before the normalization, however, post hoc t-test indicated that the P300 peak amplitude was larger only at Fz during the count compared with the motor response condition (ts 2.86, P-0.05). Therefore, scalp distribution differences among the conditions may be due to frontal activities, possibly anterior P3.
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Table 2 N250 and P300 peak amplitudes (mV"S.D.) in the count and motor response conditions
with the RT (rs0.93, P-0.05), but the P300 latency did not (rs0.64, n.s.).
Mental count
Motor response
4. Discussion
N250 Fz Cz Pz C3 C4 F39 P39
y2.90"1.48 y3.96"1.43 y2.31"0.93 y2.36"1.02 y3.24"1.13 y2.30"1.42 y2.31"0.86
y2.27"1.27 y4.18"1.43 y2.33"0.99 y2.09"0.87 y2.95"1.35 y1.52"1.13 y2.61"0.85
P300 Fz Cz Pz C3 C4 F39 P39
In the present study, we found that (1) the P170–N250–P300 complex was elicited by deviant stimuli in active-attended conditions, but not found in the ignore condition, (2) the N250 latency highly correlated with the RT and (3) the P300 peak amplitude changed between the count and motor response conditions.
4.58"1.24 5.92"1.98 5.83"2.18 5.10"1.59 4.50"1.69 4.57"1.37 5.68"1.94
*
3.19"1.54* 5.00"3.07 5.69"2.70 4.29"1.93* 4.30"2.22 3.43"1.61* 5.18"2.62
P-0.05 (count vs. motor response).
3.2.3. Relationship between ERP peak latency and reaction time Fig. 2 shows the RT and the peak latency of N250 (Cz) and P300 (Pz). The N250 peak latency was earlier than the RT in all the subjects, while the P300 peak latency tended to be later than the RT in most cases. The N250 peak latency in the motor response condition significantly correlated
4.1. N250 The N250 was not apparent in the ignore condition, whereas it was largely elicited by deviant stimuli in active-attended conditions. This result indicates that the N250 reflects active target detection in an attentive process. Kekoni et al. (1996) reported a similar result using vibratory deviant stimuli, and, therefore, suggested that the N250 might reflect the conscious target detection. Furthermore, we found the N250 in response to deviant stimuli in both the count and motor response conditions. Most of the other previous studies have also shown that the N250 was elicited by rare target stimuli (Josiassen et al., 1982; Kujala et al., 1995). However, Ito et al. (1992) and
Fig. 2. The RT and the peak latency of N250 and P300 in the motor response condition. A circle and triangle represent the data of one subject.
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Kekoni et al. (1997) reported the N250 in response to rare non-target stimuli. This may be interpreted by attentional leaking (Kekoni et al., 1996, 1997). Consistent with this idea, Kekoni et al. (1997) reported that small N250 occurred because highfrequency vibratory deviant stimuli captured the subject’s attention in an ignore condition (reading condition). Also, in Ito’s experiment non-target N250 was followed by a small P300 and slow wave, which might index involuntary shifts of attention (Kekoni et al., 1996). It may be interpreted that the attentional capturing toward deviant stimuli did not occur in the ignore condition. The fronto-central distribution of the N250 was of the same shape as the distributions of the ¨¨ ¨ auditory N2b in previous studies (Naatanen, 1992). This distribution matches well with human intracranial recordings in which the N200–P300 complex was observed from the human cingulate gyrus or frontal cortex (Baudena et al., 1995; Clarke et al., 1999; Kropotov et al., 1995; Smith et al., 1990). Kekoni et al. (1996) reported that the N250 was broadly distributed and maximal at a contralateral frontal electrode. In the present experiment, the N250 was maximal at the central electrode but we did not record at the lateral frontal site. Further investigation is needed in order to reveal the distribution of N250. Interestingly, the N250 peak latency highly correlated with the RT, whereas the P300 latency did not significantly. Furthermore, the N250 peak latency was earlier than the RT in all the subjects, while the P300 peak latency tended to be later in most cases. This result shows that the N250 is closely related to the RT and was in agreement with that of the other modalities. Unlike the P300, the auditory or visual N2 is elicited at earlier latency than the RT (Ritter et al., 1972; Renault et al., 1982). Furthermore, the N2 latency shows a strong relationship to the RT (Novak et al., 1990; Ritter et al., 1972, 1979). In contrast, although the P300 latency often correlates with the RT, sometimes it precedes the RT and sometimes it is later than the RT (Donchin and Coles, 1988). Therefore, N2 can more directly measure the absolute timing of certain processes (Ritter et al., 1979), while P300 latency reflects the stimulus evaluation time (Kutas et al., 1977; Verleger,
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1997) or post-decision closure (Desmedt, 1980). The present results are consistent with the above hypothesis of P300 latency, and show that the N250 may reflect an attentive process which controls behavioral responses in somatosensory discrimination tasks. 4.2. P300 Theoretically, P300 is an endogenous component which accompanies the context updating within the working memory stores (Donchin and Coles, 1988), and its amplitude is proportional to the amount of attentional resources devoted to a given task (Kramer and Strayer, 1988; Schubert et al., 1998; Wickens et al., 1983). One interpretation of the P300 modulation between conditions is due to working memory load. Deviant stimuli in the count condition require updates of the number within the working memory stores but not in the motor response condition. Therefore, working memory load was higher in the count compared to the motor response condition, resulting in enhanced amplitude of the P300. This assumption is consistent with the idea that the frontal association area plays an essential role in working memory, because the increase of the P300 amplitude was more remarkable at the frontal site. Furthermore, such a high working memory load would force subjects to allocate more attentional resources to a given task. Therefore, this interpretation is also in agreement with the hypothesis that the P300 amplitude reflects the amount of attentional resources. Second, it may be due to the specific allocation of attentional resources to the stimulus processing. Because subjects were asked to press a button as quickly as possible in the motor response condition, attentional resource would be allocated to not only the stimulus sequence but also the movement, whereas they only had to allocate to the stimulus sequence in the count condition. The third explanation is that the P300 modulation is based on the P3 related to the attentional orienting toward relevant stimuli. The P300 amplitude decreased especially at the frontal site in the motor response condition, suggesting that the orienting response toward relevant stimuli was suppressed by a button-pressing response.
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In the previous studies, the difference of P300 amplitude between the motor response and count tasks seems to be controversial. Johnson (1986) reported that the P300 amplitude appeared larger for a button-pressing response than for a count response. In contrast, Polich (1987) reported that the P300 amplitude was larger for a count response than for a button-pressing response. Barrett et al. (1987) also reported that the P300 amplitude was larger for a count response compared to a buttonpressing response, but this was caused by overlapping of motor-related potentials because the P300 amplitude was smaller at Cz and C3 for a buttonpressing response compared to a count response when subjects responded by pressing a button with the right index finger. Moreover, Starr et al. (1995, 1997) reported no difference in the P300 amplitude between button-pressing and silent-counting. Mertens and Polich (1997) did not seem to mention the difference of P300 amplitudes between response conditions. Although it is difficult to resolve these contradictions, at least present and previous results indicate that the P300 amplitude is sensitive to a given task. In conclusion, the present study indicated that the somatosensory N250 might reflect active target detection in an attentive process. The changes in the P300 amplitude between the mental count and motor response conditions may be related to variations in working memory load. References Baudena, P., Halgren, E., Heit, G., Clarke, J.M., 1995. Intracerebral potentials to rare target and distractor auditory and visual stimuli. III. Frontal cortex. Electroen. Clin. Neuro. 94, 251–264. Barrett, G., Neshige, R., Shibasaki, H., 1987. Human auditory and somatosensory event-related potentials: effects of response condition and age. Electroen. Clin. Neuro. 66, 409–419. Clarke, J.M., Halgren, E., Chauvel, P., 1999. Intracranial ERPs in humans during a lateralized visual oddball task; II. Temporal, parietal, and frontal recordings. Clin. Neurophysiol. 110, 1226–1244. Desmedt, J.E., 1980. P300 in serial tasks: an essential postdecision closure mechanism. Prog. Brain Res. 54, 682–686. Desmedt, J.E., Tomberg, C., 1989. Mapping early somatosensory evoked potentials in selective attention: critical evaluation of control conditions used for titrating by difference
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