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P300 Hemispheric Amplitude Asymmetries from a Visual Oddball Task

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P300 Hemispheric Amplitude Asymmetries from a Visual Oddball Task Psychophysiology, 32 (1995), 467-475. Cambridge University Press. Printed in the USA. Copyright @ 1995 Society for Psychophysiological Research P300 hemispheric amplitude asymmetries from a visual oddball task JOEL E. ALEXANDER,a BERNICE PORJESZ,b LANCE O. BAUER,c SAMUEL KUPERMAN,d SANDRA MORZORATI,e SEAN J. O'CONNOR,e JOHN ROHRBAUGH,f HENRI BEGLEITER,b ANDJOHN POLICH a a Department of Neuropharmacology, The Scripps Research Institute, La Jolla, CA, USA bDepartment of Psychiatry, State University of New York Health Sciences Center, Brooklyn, USA C Department of Psychiatry, University of Connecticut Health Center, Farmington, USA dDepartment of Psychiatry, University of Iowa, Iowa City, USA e Department of Psychiatry, Institute of Psychiatric Research, Indianapolis, IN, USA f Department of Psychiatry, Washington University, St. Louis, MO, USA Abstract The P3(OO)event-related potential (ERP) was elicited in 80 normal, right-handed male subjects using a simple visual discrimination task, with electroencephalographic (EEG) activity recorded at 19electrodes. P3 amplitude was larger over the right than over the left hemisphere electrode sites primarily at anteromediallocations (F3/4, C3/4) for target, novel, and standard stimuli. The NI, P2, and N2 components also demonstrated hemispheric asymme- tries. The strongest P3 hemispheric asymmetries for all stimuli were observed at anterior locations, suggesting a frontal right hemisphere localization for initial stimulus processing, although target stimuli produced larger P3 amplitudes at parietal locations than did novel stimuli. The relationships of hemispheric asymmetries to anatom- ical variables, background EEG activity, and neurocognitive factors are discussed. Descriptors: Event-related potentials, P3(OO),Hemispheric differences Hemispheric differences are observed readily using behavioral son, 1992; Davidson, Chapman, Chapman, & Henriques, 1990; techniques with auditory (lvry & Lebby, 1993; Kimura, 1993), Gevins et aI., 1979; Tomarken, Davidson, Wheeler, & Doss, visual (Hellige, 1993; Polich, 1993; Polich & Morgan, 1994; 1992). Further, despite a general impression that cognitive event- Sergent, 1991), and tactile (O'Boyle, van Wyhe-Lawler, & related potentials (ERPs) are fairly symmetrical in amplitude Miller, 1987; Reitan, Wolfson, & Hom, 1992) stimuli. Similar about the midline (Donchin, Kutas, & McCarthy, 1977), hemi- approaches have been employed using electroencephalographic spheric asymmetries for the P3(OO)also have been found under (EEG) measures, with consistent laterality effects obtained in task conditions that encourage differential cerebral process- a wide variety of studies (e.g., Alexander & Sufka, 1993; David- ing (e.g., Gevins et aI., 1983; Kok & Rooyakkers, 1986; Rugg & Beaumont, 1978; Schweinberger & Sommer, 1991; Tenke, Bruder, Towey, Leite, & Sidtis, 1993; van de Vijver, Kok, Bak- The Consortium on the Genetics of Alcoholism (H. Begleiter, SUNY ker, & Bouma, 1984).Thus, reliable hemispheric differences can HSCB, Principle Investigator; T. Reich, Washington University, Co- be found with behavioral and electrophysiological measures. Principle Investigator) includes six different centers where data collec- The advent of multielectrode recording and topographical tion takes place. The six sites and Principle and Co-Investigators are mapping techniques has prompted a reassessment of hemispheric Indiana University (J. Nurnberger, Jr., P. M. Conneally), University of Iowa (R. Crow, S. Kuperman), University of California-San Diego and ERP differences. In particular, several recent studies employ- The Scripps Research Institute (M. Schuckit, F. E. Bloom), University ing a relatively large number of electrodes have demonstrated of Connecticut (V. Hesselbrock), State University of New York, Health that P3 amplitude in normal subjects is greater over the right Sciences Center at Brooklyn (H. Begleiter, B. Porjesz), and Washing- than over the left cerebral hemisphere when a simple auditory ton University, St. Louis (T. Reich, C. R. Cloninger). This national oddball paradigm is used to elicit the ERPs, that is, hemispheric collaborative study is supported by the National Institute on Alcohol Abuse and Alcoholism (NIAAA) with U.S.P.H.S. grants NIAAA asymmetries are found in the absence of lateralized stimulus or UIOAA0840I, UIOAA08402, and UIOAA08403. J.E.A. was supported task influences (Alexander et aI., 1994; Holinger et aI., 1992; by NIAAA Training Grant AA07456-1Oduring the course of this work. Karniski & Blair, 1989; Naumann et aI., 1992). Additional stud- This paper is publication NP8212 from The Scripps Research Institute. ies on schizophrenic patients (and normal controls) have yielded We thank George Collins for his superlative help. similar effects (Faux et aI., 1993; McCarley et aI., 1992; Mor- Address reprint requests to: John Polich, Department of Neurophar- macology TPC-IO, The Scripps Research Institute, 10666 North Tor- styn, Duffy, & McCarley, 1993)and suggest that P3 amplitude rey Pines Road, La Jolla, CA 92037, USA. E-mail: [email protected]. from simple auditory discrimination tasks may be asymmetric 467 468 J.E. Alexander et 01. across the hemispheres. However, although such hemispheric ment, and the second electrode was located on the forehead to asymmetries have been observed they are not completely con- monitor horizontal eye movement. The filter bandpass was 0.02- sistent in their strength or location. The sources of these discrep- 50 Hz (3 dB down, 6 dB octave/slope). The EEG was digitized ancies are not clear but may be related to the nonhomogeneous at 3.9 ms/point for 1,500 ms, with a 187-ms prestimulus base- samples that are compromised by a lack of control over variables line. ERP data were averaged on line with the same computer that can affect laterality differences (e.g., left/right handedness, used to control the stimulus presentation and artifact rejec- male/female subjects, press/count tasks, etc.), the relatively tion. Trials in which the EEG or EOG exceeded :t73.3 p.Vwere small samples that are typically employed (e.g., n = 10-20), and rejected automatically. the use of linked ears or mastoids as a reference (this method ERPs were elicited with 280 stimuli presented on a computer does not appear to affect asymmetry magnitudes appreciably, monitor for a duration of 60 ms, with an interstimulus interval but it has caused some controversy in this area; cf. Andino of 1.6 s. The target stimulus was a white "X" (4 x 4 cm, 2.9° x et aI., 1990; Faux et aI., 1990; Nunez, 1981; Senulis & David- 2.9°), novel stimuli (5 x 5 cm, 3.6° x 3.6°) consisted of non- son, 1989). When taken together in this context, previous studies repeating colored geometric shapes (e.g., blue hexagons, red suggest a possible P3 hemispheric difference for nonlateralized pentagons, green triangles) arranged in variegated patterns, and stimulus presentations and simple tasks, but the nature of these the standard stimulus was a white square (4 x 4 cm, 2.9° x 2.9°). effects is still uncertain. All stimuli were viewed from a distance of 110 cm, with low The present study was conducted to ascertain whether P3 level, diffuse ambient lighting provided by a ceiling fixture. The amplitude laterality asymmetries are reliable and to assess sys- target and novel stimuli each occurred with a probability of .125; tematically the role of stimulus and task parameters on hemi- the standard stimuli occurred with a probability of .75. Subjects spheric effects. A simple visual oddball discrimination task was were instructed to focus on a dot located in the center of the employed in which stimuli consisted of an infrequently presented monitor, to press a key pad with their forefinger whenever a tar- target, infrequently presented novel patterns, and frequently pre- get stimulus was detected, and to refrain from responding when sented standards. Subjects were instructed to respond only to the novel or standard stimuli occurred. Response hand was the target stimuli and not to the other stimulus types. The infre- counterbalanced across subjects. Stimulus presentation was con- quent novel stimuli were presented to engage the discrimination cluded when 25 target, 25 novel, and 150 standard artifact-free mechanism in the absence of a response requirement but with ERP trials were acquired; time on task ranged from 7 to 10min. the same stimulus probability as the target stimulus in a manner used previously (Courchesne, 1978; Courchesne, Courchesne, Component Measurement and Analyses & Hillyard, 1978; Friedman, Simpson, & Hamberger, 1993; Waveforms for the target, novel, and standard stimuli were Pfefferbaum, Ford, Roth, & Kopell, 1980). Although presen- assessed visually and individually for each subject to identify tation of an infrequent nontarget stimulus can alter P3 scalp amplitudes and latencies of the PI, NI, P2, N2, and P3 com- distribution and peak latency in some populations (Fein & Turet- ponents at each electrode site by locating the most positive or sky, 1989; Turetsky, Raz, & Fein, 1988), this approach was negative component within the latency windows of 150-250, adopted in the present study to examine whether a response to 200-300,250-350,300-400, and 350-600 ms, respectively. Am- an infrequent stimulus contributes to P3 hemispheric differ- plitude was measured relative to the mean of the prestimulus ences. If, as suggested by auditory studies, the P3 component baseline, with peak latency defined as the time point of maxi- is larger over the right than over the left frontal regions,
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