Invited reviewUpdating P300: An integrative theory of P3a and P3b
Introduction
Discovery of the P300 spurred the use of event-related potential (ERP) methods to assess the neural underpinnings of cognition. This quest is pursued today with a convergence of methods that are beginning to hone the fundamental circuitry and identify the neurotransmitter systems activated when the P300 is observed. Although early understanding of the P300 was derived primarily from functional analysis, this once unitary phenomenon is now thought to be composed of several parts that reflect an information processing cascade when attentional and memory mechanisms are engaged. The present review develops an integrated interpretation of P300 suggested by the current neuroelectric and neuroimaging data. The groundwork is conveyed through citations and summary statements to promote an assessable still-life picture of this evolving research area.
The paper is organized into sections: first, fundamental P300 issues and a theoretical overview are presented. Second, the neuropsychological background of the P3a and P3b distinction is outlined. Third, fMRI data on P300 origins are highlighted to provide the neurophysiological foundations of component neural circuitry. Fourth, the neuropharmacological processes related to P3a and P3b are sketched to suggest how neuroelectric and neurotransmitter systems may interact. Fifth, a model system is proffered in which the P3a and P3b are proposed to result from the operation of inhibitory mechanisms engaged by incoming stimulus events to facilitate memory processing.
To maintain nomenclature consistency, the term “P300” is used to refer to the canonical ERP component, which also is called the “P3” or the more nebulous “late positive component” (LPC). The terms “P3a” and “P3b” denote the distinction between the two subcomponents as defined below. The primary empirical and theoretical approaches to P300 are covered, with early findings reviewed previously (Donchin and Coles, 1988, Hillyard and Kutas, 1983, Hillyard and Picton, 1987, Johnson, 1986, Johnson, 1988, Molnár, 1994, Picton, 1992, Price and Smith, 1974, Verleger, 1988). Not directly addressed are aging, clinical, and developmental P300 studies. These literatures have grown in specialized and cross-disciplinary ways, with summaries available elsewhere (e.g., Cycowicz, 2000, DeBoer et al., 2005, Jeon and Polich, 2003, Oken, 1997, Pan et al., 1999, Polich, 2004, Reinvang, 1999, Verleger, 2003).
Section snippets
A brief history
The P300 was first reported over 40 years ago (Sutton et al., 1965). Its discovery stemmed from the confluence of increased technological capability for signal averaging applied to human neuroelectric measures and the impact of information theory on psychological research (Sutton, 1979). The original studies manipulated stimulus information to assess how electric brain patterns varied among conditions (see Bashore and van der Molen, 1991). Subsequent results elucidated the roles of stimulus
Background
An infrequent distinct tone presented in a series of frequent tones without a task can produce a positive-going waveform having a central/parietal maximum amplitude distribution and relatively short peak latency. This component was dubbed the “P3a” to distinguish it from the task-relevant “P3b” potential elicited during target stimulus processing (Snyder and Hillyard, 1976, Squires et al., 1975). P3a from an auditory oddball task can be readily observed in about 10–15% of normal young adults (
Dual-transmitter hypothesis
The neurotransmitter systems underlying P300 generation are yet unclear, with various mechanisms implicated (Frodl-Bauch et al., 1999, Hansenne, 2000). However, available data suggest that P3a is related to frontal focal attention and working memory mediated by dopaminergic activity, and that P3b is related to temporal–parietal activity where dense norepinephrine inputs are found (cf. Braver and Cohen, 2002, Nieuwenhuis et al., 2005, Pineda, 1995, Pineda et al., 1989, Polich and Criado, 2006).
What does the P300 do?
The P300 is produced by a distributed network of brain processes associated with attention and memory operations. However, specifying a singular overarching explanation for this neuroelectric phenomenon has proven difficult, primarily because the P300 is observed in any task that requires stimulus discrimination – a fundamental psychological event that determines many aspects of cognition. Differentiation between the P3a and P3b subcomponents has begun to elucidate the interaction between
Conclusions
The present review has attempted to assess the diverse P300 literature by integrating the background findings of the P3a and P3b subcomponents. The approach traced the historical development of P300 and emphasized the functional, neurophysiological, and neuropsychological mechanisms associated with component generation. Neuroimaging and neuropharmacological investigations were highlighted to substantiate how P3a and P3b might interact. The empirical findings and developed theoretical
Acknowledgements
This work was supported by NIH Grants RO1-DA018262 and 3 P50 AA06420. It is manuscript number 18235 from The Scripps Research Institute. I thank Brendan Allison, Allen Azizian, Maya Cano, and Jonas Olofsson for helpful comments. Special thanks go to Brian Lopez for his astute editorial suggestions and figure making artistry. Sincere gratitude is expressed to the reviewers for their very perspicacious critiques.
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