Eliminating the P300 rebound in short oddball paradigms

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Abstract

In short oddball paradigms, the P3 (or P300) amplitude often shows a curvilinear “rebound” pattern, such that an initial drop during the first few trials is followed by an increase in later trials. While the initial attenuation has been attributed to habituation, no explanation has been offered for the later increase. Our hypothesis was that this curvilinear pattern is due to anticipation of the end of each fixed-length block. In study 1, a series of 16 short, fixed-length auditory oddball tests (with six targets each) replicated the rebound effect. In study 2, a further set of 16 variable-length blocks (7–10 targets) eliminated the rebound, and the P300 amplitude decreased linearly as expected. Results are interpreted in light of various constructs related to the P3: habituation, attentional salience, and updating in working memory.

Introduction

One of the best known and commonly studied event-related potential (ERP) components is the P300 (or P3). A P300 can be elicited in paradigms using any sensory modality, typically occurs approximately 300–400 ms after a deviant, infrequent, or novel stimulus, and can be manipulated through the frequency, intensity and saliency of the stimuli (Donchin and Coles, 1988). Because this ERP component is most reliable and large after infrequent, or odd stimuli (<20% occurrence), the tasks used to elicit them are often referred to as oddball paradigms.

The P300 has been found to be consistent within subjects, even over several years (Segalowitz and Barnes, 1993). However, it has also been shown to be subject to habituation effects within a test session Ravden and Polich, 1999, Romero and Polich, 1996, Pan et al., 2000. In these studies, habituation was measured across several blocks of trials spanning up to 2 h. Habituation over a shorter time span (<1 min, six to eight trials) has been investigated most thoroughly through the use of the novelty P300 paradigm.

The novelty auditory oddball is designed to examine ERPs to novel sounds embedded in a standard oddball paradigm (10% target tones, 80% nontarget tones and 10% novel auditory stimuli). Several researchers have shown that during a novelty oddball test, the amplitude of the P300 to the novel sounds diminishes more at frontal sites than at central or parietal sites over time Courchesne et al., 1975, Cycowicz and Friedman, 1997, Fabiani and Friedman, 1995, Friedman and Simpson, 1994, Kazmewrski and Friedman, 1995. Cycowicz and Friedman (1997) measured the decline of the P300 amplitude across the first 10 trials in each of eight blocks of a novelty oddball paradigm. They averaged the ERPs to the novel stimuli in pairs (1st and 2nd, 3rd and 4th, etc.) and while they report a decrease in P300 amplitude from the first to the second pair, this decrease is followed by a slight increase, although these results are not reported in detail.

Friedman and Simpson (1994) noted a curvilinear effect when comparing the P300 amplitudes to the first six novel stimuli and first six targets (deviant tones) such that for both targets and novel stimuli, the P300 amplitude declined for the first four trials, and then increased for trials 5 and 6. Thus, this P300 rebound effect appears to exist for typical targets in an oddball paradigm, as well as novel sounds.

This rebound effect seems inconsistent with the concept of habituation. It is well documented that the P300 amplitude decreases over longer testing sessions (Polich, 1989) and across multiple testing sessions with short (e.g. 1 week) inter-test intervals (Kinoshita et al., 1996). Why then would the P300 amplitude decrease initially over the first two to four trials, but increase over the next two to four trials in these short oddball paradigms?

We hypothesized that the curvilinear results found in other studies were attributable to the fixed length of each block. With only six or eight targets, the participants may have implicitly been anticipating the end of the each block, making these stimuli more salient, and this in turn influenced the P300 amplitude. We first set out to replicate these findings (study 1) and then to test our hypothesis (study 2) by using variable-length blocks, hypothesizing that the variable length blocks would eliminate this “rebound” effect in the P300 amplitude.

We expanded the typical oddball paradigm to a series of short oddball tasks employing varying different tones, but no novel stimuli. We reasoned that at the beginning of each block, the stimuli are relatively novel to the participant, and therefore the automatic adaptive orienting associated with novel-stimulus processing would occur for the initial targets. This has been previously demonstrated using a standard oddball task, where an initial increased frontality of the P300 quickly diminishes over the first few trials (Segalowitz et al., 2001). For the current study, target stimuli were changed at the start of each block. We presented 16 blocks of a standard oddball paradigm. The participant determined the target for each block by listening to the first tone (always a nontarget standard) and then only responded to tones that were different from that first tone within each block. As each new block started, attention would have to be refocussed in order to correctly categorize the tones to respond correctly. In study 1, each block was a fixed length (6 targets, 18 nontargets). In study 2, the lengths of the blocks varied randomly (7–10 targets, 21–30 nontargets).

Section snippets

Methods

Eleven undergraduate and graduate students (aged 21–31) participated. The procedures were explained in full to all participants. This study was conducted under ethical guidelines set out by the Natural Science and Engineering Research Council of Canada, and approved by the Brock University Ethics Review Board. The ERP task consisted of 16 blocks of trials, with 6 target tones and 18 nontarget tones distributed semi-randomly in each block (first two tones were always nontargets). Tones were 100

Methods

Ten undergraduate and graduate students (aged 20–33) participated. Each block began with the identical 24 tones (targets and nontargets) as the fixed-length version. However, between one and four additional targets and a proportional number of nontargets were added to each block. This resulted in 7 to 10 targets and 21 to 30 nontargets in each block. The instructions remained the same as in study 1. Trials were again averaged in sequential pairs. The 7th and 8th trials were also averaged

Discussion

We set out to modify the oddball paradigm in order to study the effect of habituation on the P300 ERP during short oddball tasks. We found that using multiple blocks of oddball paradigms of a fixed length and fixed number of targets alters the P300 amplitudes in a curvilinear way which is consistent with previous results Cycowicz and Friedman, 1997, Friedman and Simpson, 1994, and we hypothesized this may be due to implicit anticipation of the end of the test block by the participant. Cycowicz

Acknowledgements

This work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada (NSERC) to the second author. We wish to thank Tomoka Takeuchi, Patricia Pailing, Pat Moore, Mary Richard, and two anonymous reviewers for their helpful comments on earlier versions of this manuscript.

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Work performed at: Cognitive Neuropsychology Laboratory, Brock University.

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