On P300 measurement stability: habituation, intra-trial block variation, and ultradian rhythms

Biological Psychology 51 (1999) 59 – 76 www.elsevier.com/locate/biopsycho

On P300 measurement stability: habituation, intra-trial block variation, and ultradian rhythms Daran Ravden a, John Polich b,* a

Department of Psychology, St. Louis Uni6ersity, 221 North Grand Bl6d., St. Louis, MO 63103, USA b Department of Neuropharmacology TPC-10, 10550 North Torrey Pines Road, The Scripps Research Institute, La Jolla, CA 92037, USA Received 17 December 1998; received in revised form 20 February 1999; accepted 11 May 1999

Abstract P300 event-related brain potentials (ERPs) were elicited using a simple discrimination task in which participants discriminated two different equiprobable visual stimuli with buttonpress responses (n=20). A total of ten trial blocks were presented at 10-min intervals. P300 amplitude declined significantly, but peak latency did not change reliably across trial blocks. P300 amplitude demonstrated a reliable cyclical fluctuation across trial blocks, although P300 latency did not. Intra-trial block ERP variability was assessed by computing the correlation coefficients between the target and standard stimuli for amplitude and latency measures across participants within each trial block. P300 amplitude correlations were weakest at the Fz electrode, more strongly associated at Cz, and were most strongly correlated at Pz across trial blocks. P300 latency correlations were somewhat weaker and similar in strength across electrodes sites. The correlational patterns for both P300 amplitude and latency demonstrated reliable cyclical variation. The N100 component produced strong and consistent correlations for both amplitude and latency, whereas the P200 and N200 component measures evinced cyclical correlational patterns similar to the P300 across trial blocks. These results suggest that the stability of P300 and other component measures can vary appreciably within and across trial blocks in a manner that reflects ultradian variation in arousal level. © 1999 Elsevier Science B.V. All rights reserved. Keywords: Amplitude; Event-related potential (ERP); Latency; Measurement; P300; Ultradian rhythm; Variability

* Corresponding author. Tel.: + 1-858-7848176; fax: + 1-858-7849293. E-mail address: [email protected] (J. Polich) 0301-0511/99/$ - see front matter © 1999 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 1 - 0 5 1 1 ( 9 9 ) 0 0 0 1 5 - 0

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1. Introduction

1.1. P300 habituation The P300 event-related brain potential (ERP) is thought to occur when the mental model or schema of the stimulus environment is refreshed or updated (Donchin et al., 1986; Donchin and Coles, 1988). This view is similar to models proposed for orienting phenomena, such that presentation of a stimulus that is different from the preceding stimulus will reorganize attentional focus and instigate an updated representation of the stimulus environment (Sokolov, 1977; Donchin, 1981; Rohrbaugh, 1984; Simons and Perlstein, 1997). With repeated stimulus presentations in the absence of any task, clear habituation effects are observed over the first few stimulus trials for autonomic measures such as heart rate and skin conductance (Siddle et al., 1983; Verbaten et al., 1986a; Simons et al., 1987), but auditory stimuli presented in an oddball task require a relatively large number of stimulus presentations before P300 amplitude habituation is observed (Lammers and Badia, 1989; Polich, 1989; Wesensten et al., 1990). Although a similar resistance to habituation of autonomic orienting has been reported when stimuli are given ‘signal-value’ by requiring a task-relevant response (Coles et al., 1972; Berstein et al., 1975; Siddle et al., 1979), direct comparisons with the P300 from an oddball paradigm are not readily available (cf. Stephensen and Siddle, 1983; Polich, 1986b; Verbaten et al., 1986a,b; Lim et al., 1996, 1997). In addition, it should be noted that the P3a subcomponent when generated by novel auditory stimuli not requiring a response also declines rapidly with repeated presentations (Courchesne, 1978; Knight, 1984), although this effect has not been studied in task situations that tightly control the eliciting stimulus characteristics (cf. Katayama and Polich, 1998; Comerchero and Polich, 1999). In this context, it is important to note that P300 habituation from a repeated visual stimulus discrimination task has not been found consistently (cf. Tueting and Lefitt, 1979; Pritchard et al., 1986; Jodo and Inoue, 1990; Geisler and Polich, 1994; Kotchoubey et al., 1997). Because visual stimuli require more attentional resources than auditory events (Posner et al., 1976; Klein, 1977), P300 amplitude might not habituate readily for visual stimulus presentations because the stimulus and task demands are more engaging than those for auditory stimuli (Kramer et al., 1986; Polich, 1989; Strayer and Kramer, 1990; Siddle, 1991). However, differences among studies for the onset time between trial blocks also may have contributed to the inconsistency of these results. P300 habituation has not been found for visual stimuli when rel-atively long (\10-min) inter-block intervals are used (Pritchard et al., 1986; Geisler and Polich, 1994), but has generally been observed for relatively short (5 10-min) inter-block intervals (Kenemans et al., 1992; Koelega et al., 1992; Romero and Polich, 1996). If P300 amplitude habituation is affected by inter-block interval timing — perhaps because this variable modulates attentional mechanisms — then visual stimuli should also demonstrate P300 habituation effects if shorter inter-block intervals comparable to previous auditory ERP studies are employed.

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1.2. ERP measurement stability P300 measures from single-trials are relatively stable (Polich, 1986b, 1989; Polich and McIsaac, 1994; Cohen and Polich, 1997), and test-retest correlations for both peak amplitude (0.50 – 0.80) and latency (0.40–0.70) are statistically robust (Polich, 1986a; Fabiani et al., 1987; Karniski and Blair, 1989; Segalowitz and Barnes, 1993). However, a somewhat surprising consequence of repeated ERP testing is that P300 measures can fluctuate in a manner that appears related to ultradian rhythms, i.e. 90-min biological cycles (range 60–120 min) that affect human physiology and cognition (Klein and Armitage, 1979; Lloyd and Stupfel, 1991; Gordon et al., 1995; Shannahoff-Khalsa et al., 1996). Ultradian influences on ERP measures may originate from tonic changes in arousal level, which have been found to produce ultradian cycles in the EEG (cf. Manseau and Broughton, 1984; Tsuji and Kobayashi, 1988; Ortega and Cabrera, 1990). These EEG fluctuations, in turn, are thought to underlie oscillations in vigilance performance (Gertz and Lavie, 1983; Okawa et al., 1984; Treisman, 1984; Shub et al., 1997). Similarly, because arousal level is a major biological determinant of P300 (Polich and Kok, 1995), background EEG level can affect the resultant ERP so that it also reflects ultradian fluctuations (Basar et al., 1984, 1989; Basar-Eroglu et al., 1992; Polich, 1997b). Thus, arousaldriven ultradian variability in the EEG may influence ERP production in ways similar to those found in experimental studies (Sergeant et al., 1987; Klimesch et al., 1992; Mecklinger et al., 1992; Intriligator and Polich, 1995; Spencer and Polich, 1999). In this view, ultradian ERP effects could occur when P300 components are obtained with repeated testing because continual task performance becomes relatively automated as attentional engagement is reduced (Kramer et al., 1986; Polich, 1989; Strayer and Kramer, 1990). Background EEG activity in this situation would be more susceptible to biological state factors such as arousal and, therefore, reveal ultradian fluctuations in the concomitant ERP. Ultradian-like rhythms for P300 measures have been reported for re- peated trial blocks (cf. Harsh et al., 1988; Lammers and Badia, 1989; Wesensten et al., 1990; Lew and Polich, 1993; Polich, 1997a; Lin and Polich, 1999), and are not unexpected because EEG rhythms can be entrained after an initial stimulus trial block (Basar-Eroglu et al., 1992; Gordon et al., 1995). P300 measurement stability may therefore be appreciably affected by ultradian driven changes in arousal level, which can influence background EEG when repeated ERP testing is employed. Given the utility of repeated P300 assessment in applied and clinical testing (Humphreys and Kramer, 1994; Polich, 1998), it is important to characterize this variability in order to facilitate accurate ERP measurements.

1.3. Present study Given this perspective, the present study was designed to assess the related issues of visual stimulus P300 habituation, inter-trial block measurement stability, and ultradian rhythms. Short inter-block intervals and multiple trial blocks were used to

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promote P300 habituation and facilitate assessment of possible ultradian influences. All ERPs were elicited under the same stimulus probability and response conditions, so that inter-trial block as well as intra-trial block ERP variability could be measured.

2. Methods

2.1. Participants A total of 20 (ten male, ten female) young adults (mean age= 22.4, S.D.= 2.6 years) were employed. The participants reported normal health, no history of neurological or psychiatric disorders, and received course credit or monetary compensation for their participation. All participants were assessed between 10:00 and 13:00 h to minimize circadian variability, although this variable does not affect P300 measures appreciably (Geisler and Polich, 1990; Wesensten et al., 1990; Wesensten and Badia, 1992).

2.2. Stimuli and procedure Visual stimuli consisted of a checkerboard pattern or horizontal lines, viewed binocularly from a distance of 1 m. The lines were 2.5 cm (1.75°) wide, the checks were 5.0 cm (3.5°) square, and all stimuli were presented on a computer monitor with an average luminance of 35 cd/m2. Stimuli were presented in a random series once every 3 s for a duration of 100 ms each with a probability of 0.50, and the participants were instructed to look at a central fixation point during the testing period. Participants were instructed to respond to each stimulus by pressing one of two buttons with either thumb on each trial. Error rates and response times were recorded. Assignment of the arbitrary stimulus label (standard vs. target) to actual stimulus type (check vs. line) was counterbalanced across participants. A total of ten trial blocks, each consisting of at least 50 trials (i.e. 25 target and 25 standard), lasting for 6 min, were obtained from each subject (Cohen and Polich, 1997). The no-task period between the final target trial and the beginning of each subsequent block was 4 min.

2.3. Recording conditions Electroencephalographic (EEG) activity was recorded at the Fz, Cz, and Pz electrode sites of the 10 – 20 system, using gold-plated electrodes, affixed with electrode paste and tape, referred to linked earlobes with a forehead ground, and impedance at 10 KV or less. Additional electrodes were placed at the outer canthus and supraorbitally to the left eye, with a bipolar recording made of electro-ocular activity. The filter bandpass was 0.016–30 Hz (3 dB down, 12 dB octave/slope). The EEG was digitized at 3 ms per point for 768 ms, with a 75-ms pre-stimulus baseline.

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Waveforms were averaged online by a commercial signal averager, which also controlled the stimulus presentation and artifact rejection. Trials on which the EEG or EOG exceeded 9 90 mV were rejected automatically, and stimuli were presented until the total number for each stimulus was acquired (with approximately 5% rejected overall).

3. Results All analyses of variance employed Geisser-Greenhouse adjustments to the degrees of freedom, with only the probability values from the corrected df reported here. Simple main effects and Newman–Keuls comparisons were used for post-hoc comparisons, with polynomial multiple regression procedures employed to assess the reliability of ERP cyclical variation.

3.1. Task performance The overall error rate was 0.5%. A two-factor (two stimulus types× ten trial blocks) analysis of variance applied to the error rate found no significant effects or interactions. RT did not differ between stimulus types (P\ 0.70) and became marginally shorter from the first to the tenth trial block (from 420 to 390 ms, respectively), with F(9,171) = 2.4, PB 0.10. In sum, participants responded to the discrimination task accurately and somewhat more quickly across trial blocks.

3.2. ERP habituation analyses Fig. 1 illustrates the grand averaged target and standard stimulus ERPs for each trial block and electrode site. The ERP waveforms were analyzed by defining the P300 component as the maximum positive peak occurring after the N100-P200N200 components within the latency window 300–600 ms. The amplitude and latencies of the N100, P200, and N200 components were assessed by measuring the largest negative or positive potential within the latency windows 80–180, 175–300, and 250 – 400 ms, respectively. Amplitude was measured relative to the prestimulus baseline, and peak latency was defined as the time of the maximum positive point. Fig. 2 presents the mean P300 amplitude and latency values for each trial block at each of the three scalp recording sites. Inter-trial block changes were assessed with a three-factor (two stimulus types× ten trial blocks× three electrodes) analysis of variance that was applied to the amplitude and latency data from each component. Table 1 summarizes the results of these analyses.

3.2.1. P300 component As expected, no reliable differences between the arbitrarily assigned target and standard stimulus label conditions were obtained (P\ 0.15). The stimulus type×

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Fig. 1. Grand averaged event-related potentials from the target and standard stimuli for each trial block and electrode site (n= 20).

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trial block number (P \ 0.50), stimulus type× electrode (P\0.60), and the threeway (P \ 0.85) interaction were all non-significant. Simple effects tests revealed a marked decrease in amplitude across trial blocks at the Fz electrode, F(9,265)= 2.8, PB 0.01; a somewhat weaker effect at the Cz electrode, F(9,265)= 2.2, P B 0.05; and a non-significant decline for the Pz electrode (FB 1, P\ 0.65). P300 amplitude increased from the frontal to parietal electrode sites, with Newman–Keuls post-hoc comparisons verifying that mean amplitudes from the Fz electrode were smaller than those from the Cz electrode (PB 0.001); the Fz and Cz electrodes were smaller

Fig. 2. Mean target (open symbols, solid line) and standard (closed symbols, dashed line) P300 amplitudes and latencies for each electrode as a function of trial block.

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Table 1 Summary of F-ratios from analyses performed on component amplitudes and latencies Factor (df)

Stimulus type (1,19) Trial block (9,171) Electrode site (2,38) S×B (9,171) S×E (2,38) B×E (18,342) S×B×E (18,342)

Amplitude

Latency

N100

P200

N200

P300

N100

P200

N200

P300

– – 15.8*** – – – –

– 2.4* – – – – –

– – – – – 2.6* –

– 3.7** 29.4*** – – 2.3* –

– – – 2.4* – – –

– 3.0* 5.6** – – – –

– 3.1* 6.2** – – – –

– – – – – – –

* PB0.05. ** PB0.01. *** PB0.001.

than those from the Pz electrode (PB 0.001 and PB 0.05, respectively). P300 latency produced no reliable habituation effects. Analysis of the cycle-like P300 amplitude and latency fluctuations apparent in Fig. 2 are presented below.

3.2.2. N100, P200, and N200 components These potentials were evaluated (here and below) to ascertain the degree to which the obtained effects were independent of the P300 component. Table 1 presents the results for the other ERP components. The amplitude and latency values from each stimulus type were not different for these components. N100 latency evinced a significant stimulus type × trial block interaction, although this result appeared to originate from non-systematic variation, no discernible pattern could be found across trial blocks. P200 amplitude declined across trial blocks; N200 amplitude demonstrated a significant trial block×electrode interaction, although no systematic trends were observed. P200 and N200 latency tended to decline with trial block. In general, the trial-block habituation effects for the other components were less consistent compared to the P300, as has been observed previously for auditory stimuli (Polich, 1989; Lew and Polich, 1993). 3.3. Intra-trial block correlations Intra-trial block variability was assessed by computing Pearson’s correlation coefficients between the ‘target’ and ‘standard’ stimulus values across participants for the amplitude and latency measures. Fig. 3 illustrates the target/standard stimuli correlations as a function of trial block for P300 amplitude and latency values at the Fz, Cz, and Pz electrode sites. Fig. 4 presents the correlations as a function of trial block for the N100, P200, and N200 amplitude and latency values for each electrode site. The horizontal dotted line in each figure denotes the r-value at which statistical significance is reached (df= 18, PB 0.05, two-tail test). These figures

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indicate that the P300 and other components demonstrated considerable within-block variability across the ten trial blocks. However, it is worth noting that the P300 amplitude and latency intra-trial correlation for the first block are exactly the same as those observed for test-retest reliability (Polich, 1986a; Segalowitz and Barnes, 1993); hence, these intra-block effects are identical to test-retest measures. These within-block correlations were then analyzed in two different ways as described below.

Fig. 3. Correlation coefficients between the target and standard stimulus P300 measures for amplitude (top) and latency (bottom) from each electrode and trial block. The dotted line denotes the statistical significance level (df =18, PB 0.05, two-tail test).

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Fig. 4. Correlation coefficients between the target and standard stimulus N100, P200, and N200 measures for amplitude (top) and latency (bottom) from each electrode and trial block. The dotted line denotes the statistical significance level (df =18, P B0.05, two-tail test).

3.3.1. Electrode comparisons The amplitude and latency correlation coefficients for each component from each electrode and trial block were transformed using the Fisher-z method to normalize the r distribution. A one-factor (electrode site) analysis of variance was applied to the transformed r values from each measure. P300 amplitude yielded an overall significant difference among electrodes, F(2,18)= 27.2, PB 0.001. Newman–Keuls post-hoc comparisons found that the mean correlation from the Fz electrode was significantly less than that from Cz (PB 0.002) and Pz (PB 0.001) electrodes; the mean correlation from Cz was less than Pz (PB 0.002). P300 latency correlations demonstrated no overall difference among the electrodes (P\ 0.35, in all cases). The same analysis was applied to the ERP values from the other components. N100 amplitude yielded a significant electrode effect, F(2,18)= 4.9, PB 0.05; Fz produced a smaller mean correlation than Pz (PB 0.02); and Cz was smaller than Pz (P B0.05). N100 latency correlations were not reliably different from one another (P \0.10, in all cases). P200 amplitude correlations were significantly different among electrodes, F(2,18)= 6.8, PB 0.02. Fz evinced smaller mean correlations than Cz (P B0.01), and Cz was less than Pz (PB 0.01). P200 latency

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(P\0.15), N200 amplitude (P\ 0.10), and N200 latency (P\ 0.80) correlational differences among electrodes were not obtained.

3.4. Ultradian rhythm analyses 3.4.1. ERP inter-trial block 6ariation To determine whether the fluctuating P300 measures across trial blocks illustrated in Fig. 2 were reliable, component amplitude and latency (i.e. using the mean of the target and standard stimulus values) were analyzed using polynomial regression, with trial block as the independent variable. The R 2 values and F-test for the statistically strongest polynomial equation for each component are reported below. 3.4.2. P300 component As expected, amplitude measures yielded significant linear trends for each electrode (P B 0.05 in all cases). More important, however, were the findings that appreciably more variance was accounted for by polynomial trends. Fz amplitude was best fit with a significant 4th order polynomial, R 2 = 0.925 and F(4,5)= 15.4, PB 0.005; Cz amplitude yielded a significant 4th order polynomial, R 2 = 0.953 and F(4,5) = 25.1, P B 0.002; Pz amplitude demonstrated a marginal 4th order polynomial, R 2 =0.804 and F(4,5) = 5.1, PB 0.052. As suggested by the more variable patterns for P300 latency in the lower panel of Fig. 2, no significant regression equations were obtained. These outcomes mimicked the overall P300 habituation analysis in that the significant polynomial effects were found only for the amplitude data. If individual participants became similarly task-engaged at about the same point in time after the initial trial block—a phenomenon that also has been reported for cognitive measures repeated across time (Gordon et al., 1995; Shub et al., 1997) — a 90-min ultradian rhythm would manifest itself such that one cycle (plus the additional time-on-task from the tenth block) would yield a 4th or 5th order polynomial trend. Thus, the significant P300 amplitude quartic trends appear to reflect reliable ultradian-related changes in ERP task processing. 3.4.3. Other ERP components The N100, P200, and N200 data from the Cz electrode were analyzed similarly. N100 latency yielded a significant 4th order polynomial, R 2 = 0.898 and F(4,5)= 11.0, P B0.01; P200 amplitude produced a significant 4th order polynomial, R 2 = 0.823 and F(4,5) =5.8, PB 0.05. N200 demonstrated no significant polynomial effects. In general, the patterns for these components also reflected those found for the habituation analyses of these components. 3.4.4. Intra-trial block correlations To determine whether the cyclical patterns of the within-trial block correlations apparent in Figs. 3 and 4 were statistically meaningful, the correlation coefficients (the r-values were not transformed to preclude exaggerating any trends) from each electrode across trial blocks were analyzed using polynomial regression. The R 2

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values and F-test for the statistically strongest polynomial equation are reported for each component and electrode. Because the correlational patterns varied in degree and strength among electrode sites, statistical results are also reported when all of the beta coefficients (i.e. strength of the polynomial factors) were significant, even though the overall regression F-test may not have been. This approach was adopted because the relevant polynomial effects (cubic, quartic, quintic) accounted for a large proportion of variance in the most significant equation and, therefore, index trends consistent with ultradian influences on ERP measures. Moreover, the correlational outcomes in Figs. 3 and 4 evince considerable similarity with respect to the cyclical patterns, suggesting that the same mechanism was operating to produce these effects. Thus, the significant contribution of the polynomial trends warranted reporting of these outcomes, even though the overall regression analysis was marginal or was not strong enough to attain significance. P300 amplitude intra-block correlations from the Fz electrode were best fit with a 5th order polynomial, R 2 =0.778 and F(5,4)= 2.8, PB 0.20, with all beta coefficients significant and thereby reflecting reliable linear, cubic, quartic, and quintic contributions to the overall equation (PB 0.05). Cz electrode amplitude yielded a 4th order polynomial, R 2 = 0.683 and F(4,5)= 2.7, PB 0.20, with all beta coefficients significant (P B0.05). Pz amplitude correlations were best fit with a significant 4th order polynomial, R 2 = 0.826 and F(4,5)= 5.9, PB0.05, with all beta coefficients significant (P B 0.05). P300 latency from the Fz electrode produced a 5th order polynomial, R 2 =0.875 and F(5,4)= 5.6, PB 0.06, with all beta coefficients significant (P B 0.05). Cz latency electrode data yielded a 3rd order polynomial, R 2 =0.638 and F(3,6)= 3.5, PB 0.10, with all beta coefficients significant (P B0.05). Pz latency did not demonstrate reliable polynomial effects (P \ 0.25 for the cubic, quartic, and quintic trends). In sum, these analyses indicate that the curvilinear relationships for P300 target/standard correlational strength across trial blocks (time-on-task) were systematic and generally statistically reliable. N100 amplitude and latency correlations did not produce any significant polynomial outcomes. P200 amplitude from the Cz electrode evinced a significant 4th order polynomial, R 2 = 0.832 and F(4,5)= 6.2, PB0.05, with all beta coefficients significant (P B0.05). P200 latency from the Cz electrode produced a 4th order polynomial, with all beta coefficients significant (PB 0.05), R 2 = 0.772 and F(4,5) = 4.2, PB 0.10. N200 amplitude at Fz produced a significant 4th order polynomial, R 2 = 0.819 and F(4,5)= 5.7, PB 0.05. The Cz electrode data were less robust, R 2 = 0.666 and F(4,5)= 2.5, PB 0.20, but all of the beta coefficients were significant (PB0.05). N200 latency from Cz yielded a 4th order polynomial, R 2 =0.758 and F(4,5)= 3.9, PB 0.10, with all of the beta coefficients significant (P B 0.05). These findings suggest that the curvilinear patterns from the P200 and N200 target/standard correlations across trial blocks were systematic and statistically reliable in a manner similar to the P300 component data.

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4. Discussion

4.1. P300 amplitude habituation P300 amplitude habituated across trial blocks, with the strongest decreases occurring at the Fz and Cz electrode sites. P300 latency did not demonstrate habituation effects. P300 from visual stimuli has been reported to decline in amplitude in some paradigms (Kok and Loreen de Jong, 1980; Verbaten et al., 1986a,b; Kenemans et al., 1988; Kotchoubey et al., 1997), but has not been found when participants are required to engage in an active discrimination task (cf. Tueting and Lefitt, 1979; Pritchard et al., 1986; Jodo and Inoue, 1990; Geisler and Polich, 1994; Romero and Polich, 1996). The present findings emphasize the critical importance of inter-trial block interval for visual stimulus P300 habituation and suggest a theoretical link between attentional resource allocation and ERP habituation: short inter-block intervals facilitate automization of the two-choice discrimination task by requiring fewer attentional resources as time-on-task increases so that smaller P300 amplitudes are obtained (Kramer et al., 1986; Polich, 1989), at least for the relatively simple task employed here (cf. Strayer and Kramer, 1990; Kok, 1990, 1997). Thus, P300 habituation with visual stimuli is obtained with successive trial blocks and short inter-block intervals. P300 habituation was strongest at the Fz and Cz electrode sites but dissipated at the Pz electrode site. This outcome implies that P300 habituation occurs primarily over fronto-central areas, as similar patterns for auditory stimuli also have been reported (Polich, 1989). Given this result, stimulus discrimination could engage frontal lobe activation as a consequence of attentional focus—a major attribute of frontal lobe function — but deteriorate with extensive time-on-task (Posner and Petersen, 1990; Pardo et al., 1991; Posner, 1992; Potts et al., 1996; McCarthy et al., 1997). The marked frontal P300 decrease may therefore stem from a decreased frontal lobe response to alerting stimuli, since P300 generation in a discrimination task appears to initially engage frontal activity that may decline after multiple repetitions of task requirements (Courchesne, 1978; Polich et al., 1997). Furthermore, even though the present visual stimulus discrimination was not designed expressly to elicit a separate P3a subcomponent, it is reasonable to suppose that the stronger habituation effects observed for the fronto-central electrodes may reflect habituation of the P3a portion to the overall P300 (i.e. P3b) amplitude (cf. Knight, 1984, 1996; Katayama and Polich, 1998). The present effects would therefore seem to imply that even a simple two-choice task can index the operation of multiple sources to the obtained P300 ERP in such tasks (Squires et al., 1975; Verleger et al., 1994). However, regardless of the exact neural or cognitive underpinnings, it is important to emphasize that when ERPs are obtained under re-peated testing conditions, as is often the case for applied or clinical purposes, variation in P300 measures related to habituation effects needs to be considered to ensure accurate evaluation of the results (Humphreys and Kramer, 1994; Polich, 1998).

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4.2. ERP measurement stability In addition to the significant P300 amplitude decreases observed across trial blocks, statistically reliable cyclical patterns were also found. These findings suggest that ultradian fluctuations occur when participants repeatedly engage in discrimination task performance. Cyclical variation of P300 over trial blocks has been observed previously, albeit not consistently, perhaps because of differences in inter-trial block interval among studies (cf. Lammers and Badia, 1989; Wesensten et al., 1990; Lew and Polich, 1993; Kotchoubey et al., 1997; Polich, 1997a; Lin and Polich, 1999). More important, the intra-trial block correlational patterns portrayed in Fig. 3 indicate that P300 amplitude from the frontal-central electrodes produced less consistent intra-trial block component measures than the parietal electrode site. If this assumption is accurate, these findings imply that the P3a subcomponent of the P300 from frontal-central recording areas is sensitive to ultradian influences and may index ultradian-driven variation stemming from fluctuations in arousal level and cognitive performance (Klein and Armitage, 1979; Kok, 1990; Gordon et al., 1995; Polich and Kok, 1995; Shannahoff-Khalsa et al., 1996; Shub et al., 1997). P300 latency also evinced cyclical fluctuations of intra-trial block variation with sufficient strength to produce significant polynomial patterns. Because EEG power and P300 amplitude are associated (Basar et al., 1984, 1989; Basar-Eroglu et al., 1992; Mecklinger et al., 1992; Intriligator and Polich, 1995; Polich, 1997a,b; Spencer and Polich, 1999), it is reasonable to suppose that the inter- as well as intra-trial block cyclical ERP variation is related to ultradian rhythms. These ERP effects may occur at least in part because frontal lobe alerting mechanisms are sensitive to arousal state (cf. Posner, 1992; Potts et al., 1996; McCarthy et al., 1997). Although speculative, the nature and locus of the observed fluctuations are consistent with the wide range of ultradian findings and similar outcomes from previous P300 studies. Thus, analysis of intra-trial block P300 variation may provide a sensitive means of assessing biological influences and improve applied and clinical ERP measurements.

5. Conclusion The present ERP findings demonstrate P300 habituation for visual stimuli and reliable cyclical fluctuations for correlations between and within target/standard amplitude and latency measures at the frontal-central electrode sites. The systematic and statistically reliable inter- and intra-trial block variation observed may reflect fundamental biological variability related to ultradian influences associated with changes in arousal state. Additional assessment of these effects is needed to refine measurement of the P300 and other ERPs to increase their reliability and sensitivity in applied testing.

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Acknowledgements This work was supported by NIDA grant RO1-DA08363-03 and is publication number NP11562 from The Scripps Research Institute.

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