P3a and P3b from typical auditory and visual stimuli

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Abstract

Objective: Target/standard discrimination difficulty was manipulated systematically to assess how this variable affects target and nontarget P300 scalp distributions for both auditory and visual stimuli.

Design and methods: A 3-stimulus paradigm (target, standard, nontarget) was employed in which subjects (n=16) responded only to an infrequently occurring target stimulus. The perceptual discrimination difficulty between the target and more frequently occurring standard stimuli was varied as Easy or Difficult in different conditions, while holding the nontarget stimulus properties constant.

Results: When target/standard discrimination was Easy, P300 amplitude was larger for the target than the nontarget across all electrode sites, and both demonstrated parietal maximums. In contrast, when target/standard discrimination was Difficult, target amplitude (P3b) was larger parietally and occurred later than nontarget components, whereas nontarget amplitude (P3a) was larger and earlier than the target P300 over the frontal electrode sites. Similar outcomes across task conditions were obtained for both auditory and visual stimuli.

Conclusions: The findings suggest that target/standard discrimination difficulty, rather than stimulus novelty, determines P3a generation for both auditory and visual stimulus modalities.

Introduction

In many event-related brain potential (ERP) studies, the P300 component is obtained with the so-called `oddball' paradigm, wherein two stimuli are presented with different probabilities in a random order. The subject is required to discriminate the infrequent target stimulus from the frequent standard stimulus by noting the occurrence of the target, typically by pressing a button or mentally counting. The P300 elicited by the target stimulus in this task is a large, positive-going potential that is of maximum amplitude over the parietal electrode sites with a peak latency of about 300–350 ms for auditory and 350–450 ms for visual stimuli in normal young adults (Johnson, 1988; Picton, 1992). This brain potential is thought to reflect attentional resource allocation when working memory is engaged and despite its simplicity, has provided a great deal of information about the neural activity underlying fundamental cognitive operations (Donchin and Coles, 1988; Polich, 1998).

The `3-stimulus' paradigm is a modification of the oddball task in which infrequent-nontarget stimuli are inserted into the sequence of target and standard stimuli. When `novel' stimuli (e.g. dog barks, color forms, etc.) are presented as infrequent nontarget stimuli in the series of more `typical' target and standard stimuli (e.g. tones, letters of the alphabet, etc.), a P300 component that is large over the frontal/central areas is produced with auditory, visual, and somatosensory stimuli (Courchesne et al., 1984; Knight, 1984; Yamaguchi and Knight, 1991). This `novelty' P300 is sometimes called the `P3a,' whereas the parietal maximum P300 from the target stimulus is sometimes called the `P3b' (Courchesne et al., 1975; Squires et al., 1975). Because the P3a exhibits an anterior/central scalp distribution, a relatively short peak latency, and habituates rapidly, it has been interpreted as reflecting frontal lobe function (Friedman et al., 1993; Friedman and Simpson, 1994; Knight, 1996).

In another variant of the 3-stimulus paradigm, infrequent-nontarget `typical' visual stimuli that are easily recognized (i.e. not novel) have been found to elicit a P300 with maximum amplitude over the central/parietal rather than frontal/central areas (Courchesne, 1978; Courchesne et al., 1978). This component is sometimes referred to as a `no-go' P300, because subjects do not respond to the infrequent nontarget. Infrequent nontarget auditory tone stimuli (i.e. not novel) inserted into the traditional oddball sequence will elicit a parietal maximum P300 that is smaller and later than the target P300 (Pfefferbaum et al., 1980; Pfefferbaum and Ford, 1988). Thus, for both the visual and auditory modalities, the novel stimuli elicit a central maximum P300 whereas infrequent nontarget stimuli elicit a central/parietal P300 (cf. Grillon et al., 1990; Verbaten et al., 1997).

Although distinguishing among the various P300 potentials is of theoretical and empirical importance, systematic assessments of the 3-stimulus paradigm are few. Katayama and Polich (1996b)manipulated target and nontarget stimulus probability in an auditory 3-stimulus paradigm and obtained highly consistent results for both target and nontarget stimuli: P300 components from the nontarget tones were essentially the same as those from target stimuli, and P300 target stimulus measures were unaffected by the probabilities of either the standard or nontarget stimuli. A second study compared target stimulus P300 from 3-, 2-, and single-stimulus auditory paradigms and found similar components across tasks (cf. Katayama and Polich, 1996a; Polich and Heine, 1996; Mertens and Polich, 1997). These findings indicate that P300 components from target and nontarget stimuli are both affected by stimulus probability variation even though only the target stimulus requires a response.

Katayama and Polich (1998)assessed the role of task difficulty to examine more closely the effects of stimulus context on P300 component scalp distribution. In this study, the perceptual distinctiveness between the target and standard stimuli was manipulated in an auditory 3-stimulus task by using typical tone stimuli that varied in pitch. When the target/standard discrimination was easy and the nontarget/standard difference was large, P300 target amplitude was larger than nontarget amplitude across the midline electrode sites, and both component types were largest over the parietal sites. However, when target/standard discrimination was difficult and the nontarget/standard difference was large, the nontarget stimulus elicited a P300 that was greater in amplitude frontally and shorter in latency than the target P300, findings remarkably similar to those previously reported when `novel' nontarget stimuli have been employed (Courchesne et al., 1975, Courchesne et al., 1978; Courchesne, 1978; Friedman et al., 1993).

Taken together, these results imply that when the perceptual discrimination between the target and standard stimulus is difficult, increased frontal/central amplitude for the infrequent nontarget P300 (P3a) and a parietal maximum for the target P300 (P3b) are obtained. Theoretically, this outcome suggests that the P3a vs. P3b distinction emerges because the stimulus context defines the degree of attentional focus required for the primary discrimination task, which is interrupted by an infrequently occurring nontarget stimulus event. When considered with the P3a/P3b findings reviewed above, it is reasonable to suppose that stimulus context – the relative perceptual distinctiveness among stimuli – affects both target and nontarget P300 amplitude because these components are generated by different neural structures Indeed, correlations between magnetic resonance imaging (MRI) gray matter volume measurements and P300 amplitude demonstrate distinct regional differences: frontal areas produce stronger associations with nontarget startling stimuli, and parietal areas produce stronger associations with target stimuli (Ford et al., 1994). Additional ERP and MRI findings also indicate frontal lobe activity for the detection of rare but alerting stimuli (Knight, 1996, Knight, 1997; Potts et al., 1996; McCarthy et al., 1997; Polich et al., 1997; Verbaten et al., 1997). Thus, P300 amplitude from different stimulus contexts appears to reflect brain areas that are related to specific stimulus evaluation processes.

If stimulus context determines P3a/P3b generation in the manner outlined above, then the nontarget P300 should be affected by the magnitude of the target/standard perceptual difference for the auditory and visual modalities as has been found for novel and no-go paradigms: Easy target/standard discrimination should produce parietal maximum P300 distributions, whereas difficult target/standard discrimination should produce greater frontal P300 amplitude (Friedman and Simpson, 1994; Verbaten et al., 1997; Katayama and Polich, 1998). In this view, the nature of the stimulus context will direct attentional focus such that an infrequent nontarget stimulus will interrupt the processing operations employed in a difficult target/stimulus discrimination and engage frontal lobe activity much more forcefully compared to a relatively easy discrimination task.

Section snippets

Subjects

A total of 16 young adults (8 male, 8 female) served as subjects (mean age 21.4, SD 1.4 years) and received course credit or pecuniary remuneration for their participation. All subjects reported being free of neurological and psychiatric disorders and provided written, informed consent.

Recording conditions

Electroencephalographic (EEG) activity was recorded at the Fz, Cz, and Pz electrode sites, referred to linked earlobes, with a forehead ground and impedance at 10 kΩ or less. Additional electrodes were placed at

Task performance

Table 2 summarizes the performance data from all task conditions. A two-factor (2 modalities×2 difficulty levels) multivariate analysis of variance (MANOVA) was performed on the response time (RT) from the target stimuli. RT for the Easy tasks was significantly shorter than for the Difficult tasks, F(1,15)=57.6, P<0.001. Target hit rate was significantly higher in the Easy tasks than in the Difficult tasks, F(1,15)=31.6, P<0.001. No interactions were obtained for either analysis. The false

Discussion

Response time and hit rate results confirmed the successful manipulation of task difficulty by varying the degree of perceptual discrimination between target and standard stimuli. When the target was physically similar to the standard, reaction time increased and hit rate decreased compared to when the target was very different from the standard. Although these task difficulty effects were somewhat stronger for the auditory compared to visual stimulus conditions for RT, the ERP outcomes were

Acknowledgements

This study was supported by an Undergraduate Research Scholarship to the first author from the Committee on Undergraduate Scholarships and Honors, University of California, San Diego, and NIDA Grant DA08363 to J.P. We thank Dr. Aaron Ilan for his helpful comments with earlier versions of this paper. This is manuscript NP11058 from The Scripps Research Institute.

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