BEHAVIORAL BIOLOGY 16, 319-331 (1976), Abstract No. 5268
Long-Latency Evoked Potentials to Irrelevant, Deviant Stimuli 1
E L A I N E S N Y D E R and STEVEN A. H I L L Y A R D
Department o f Neurosciences, University o f California, San Diego, La Jolla, California 92093
Occasional shifts of loudness in a repetitive train of clicks elicited a late-positive wave (P3a) in nonattending subjects which peaked at a mean latency of 258 msec and had a fronto-central scalp distribution; and P3a was typically preceded by an "N2" component at 196 msec. The P3a wave was distinguishable from the longer-latency (378 msec) parieto-centrally distributed "P3b" wave, that was evoked by the same stimulus in an actively attending subject, thus confirming the findings of Squires et al. Infrequently presented single sounds did not produce large or consistent N2-P3a components; the critical condition for the generation of an N2-P3a wave seemed to be that the infrequent sounds represent a deviation (intensity increment or decrement) from a repetitive background. Furthermore, increasing the repetition rate of the background clicks drastically reduced N1-P2 amplitude but had little effect on the amplitude of N2-P3a. This suggests that N2-P3a is not simply a delayed N1-P2 "vertex potential," but rather reflects the operation of a "mismatch" detector, which registers deviations from an ongoing auditory background.
When a subject attends to a train of repetitive auditory stimuli in order to detect an i n f r e q u e n t "target" stimulus such as a pitch change (Ritter et al., 1972), i n t e n s i t y sbdft (Ritter and Vaughan, 1969; P i c t o n and Hillyard, 1974), or o m i t t e d stimulus (Picton et al., 1974; P i c t o n and Hillyard, 1974) w i t h i n that train, the averaged evoked potential (EP) to the target stimuli selectively develops an e n h a n c e d late positive wave (P3 or P300). This P3 wave, peaking at a latency of 3 0 0 - 4 5 0 msec, has most generally been interpreted as a neural correlate o f decision m a k i n g or signal d e t e c t i o n by an actively attending subject (Hillyard, 1969; Smith et al., 1970; Hillyard et al., 1971; Paul and S u t t o n , 1972). On the other hand, several authors (Ritter et al., 1968; R o t h , 1973; R o t h and Kopell, 1973; R o t h et al., 1973) have reported that a " P 3 " 1This work was supported by NIH Grant MH-25594-01 to S. A. Hillyard and NASA Grant NGR 05-009-198 to R. Galambos and was conducted while E. Snyder held a Sloan Foundation Fellowship. Address reprint requests to Elaine Snyder, Department of Neuroscience (A-012), University of California, San Diego, La Jolla, California 92093. 319 Copyright © 1976 by Academic Press, Inc. All rights of reproduction in any form reserved.
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wave can also occur to infrequent, unpredictable stimulus changes under conditions where the subject is instructed to ignore the stimuli altogether. In an attempt to resolve this apparent inconsistency m the P3 literature, Squires, Squires, and Hillyard (1975) presented evidence that two distinct varieties of P3 waves (tentatively labeled "P3a" and "P3b") can be elicited depending on the circumstances. The "P3a" wave was evoked by "deviant" stimuli (pitch or intensity shifts) within a train of "standard" tone pips, whether they were being attended or not: this wave occurred earlier than the "classic" 300 msec (mean latency 265 msec) and had a fronto-central scalp distribution. In contrast, the P3b component was evoked only when the subject attended to the train of stimuli and performed some kind of response to the "deviant" stimuli (e.g., counted them). Moreover, the P3b wave had a scalp distribution with a parieto-central maximum amplitude and a mean latency of around 250 msec. The P3b seems to correspond in latency and topography to the "P3" reported in most prior studies (e.g., Ritter et al., 1972; Hillyard et al., 1976), while a late wave resembling the P3a appears in reports from Roth's laboratory (e.g., Roth, 1973). The identification of two varieties of late positive "P3" waves has helped to clarify some of the discrepancies in the literature but the nature of the P3a wave itself is little understood. Squires et al. (1975) noted that the P3a could be elicited by several types of deviant stimuli in an ongoing tram and suggested that P3a indexes a "mismatch" detection or "a basic sensory mechanism which registers any change in a background stimulus." Other interpretations still remain tenable, however. First, it may be that P3a represents activity of a neuronal population with a long refractory period that is specifically activated by the infrequent stimulus, whether or not it occurs by itself or as a deviation from an ongoing train. Because of its long refractory period, a P3a would not be evoked by the more frequent stimuli in the train. Squires et al. (1975) considered this interpretation unlikely since a rare intensity decrement in a train which elicited a large P3a would not be likely to activate a nonrefractory neural population separate from the one activated by the louder repetitive stimulus. Nonetheless, present evidence does not definitely rule out this possibility. A second hypothesis to be considered is that the P3a does not represent neural activity specific to a rare or deviant stimulus, but rather has a neural generator in common with the earlier P2 component of the auditory vertex potential; in this case, the deviant stimulus must act to delay the P2 by some 60-80 msec from its normal latency of 160-180 msec. In this connection, Squires et al. (1975) noted that the P3a was frequently preceded by an "N2" component at 180-200 msec, which might then represent a delayed Nl wave of the vertex potential. The present experiment was designed to explore these alternative interpretations of the recently-identified P3a component. To determine if P3a is simply a stimulus-specific component with a long refractory period,
EVOKED POTENTIALS TO IRRELEVANT, DEVIANT STIMULI
321
auditory EPs were compared when infrequent stimuli (clicks) were presented alone, as opposed to being embedded in repetitive trains of clicks of a different intensity. To find out whether the P3a generator can be dissociated from that of P2, the repetition rate of the ongoing train was manipulated, a procedure well known to influence P2 amplitude (Davis et al., 1966; Nelson and Lassman, 1968). If P3a reflects a straightforward mismatch detection operation, however, it might be expected to be relatively insensitive to stimulus repetition rate and thus dissociable from P2.
METHOD Subjects Twelve normal young adults (18-32 yr; 10 male and 2 female) served as subjects. Six of the subjects were naive as to the purpose of the experiment, four were laboratory personnel, and two were the authors. Stimuli The stimuli consisted of binaural clicks generated by passing 100/~sec square waves through earphones; the clicks were either "loud" (65 db SL) or "soft" (55 db SL) in intensity. Two basic types of stimulus sequences were used. In the first, clicks were given regularly at a fixed rate of 1/sec, 2/sec, or 3/sec in different blocks of the experiment; each block lasted five minutes. Within each block, 90% of the clicks were of one intensity (designated the "standard") while the remaining 10% were of the other intensity (designated the "rare" stimulus, which was interspersed at random in the sequence). Each block of trials contained a total of 32 rare stimuli. In the second type of stimulus sequence, the 32 rare stimuli were presented alone, at interstimulus intervals that were identical to those when the intervening standard stimuli were present. In all there were eight types of stimulus sequences: six with repetitive trains of stimuli (having loud and soft intensities as rare stimuli at each of three repetition rates), and two with rare stimuli presented alone (loud and soft stimuli). Procedure The subject was seated in a reclining chair and was instructed to minimize eye movements and blinks throughout the periods of stimulation. The eight stimulus sequences were administered in separate blocks with the subject reading a book under instructions to ignore the clicks ("inattend" condition). An additional two blocks of stimuli were given at the 1/sec rate while the subject counted the number of rare clicks within each block ("attend" condition); one of these sequences used soft rare clicks, the other
322
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Long-Latency Evoked Potentials to Irrelevant, Deviant Stimuli 1
E L A I N E S N Y D E R and STEVEN A. H I L L Y A R D
Department o f Neurosciences, University o f California, San Diego, La Jolla, California 92093
Occasional shifts of loudness in a repetitive train of clicks elicited a late-positive wave (P3a) in nonattending subjects which peaked at a mean latency of 258 msec and had a fronto-central scalp distribution; and P3a was typically preceded by an "N2" component at 196 msec. The P3a wave was distinguishable from the longer-latency (378 msec) parieto-centrally distributed "P3b" wave, that was evoked by the same stimulus in an actively attending subject, thus confirming the findings of Squires et al. Infrequently presented single sounds did not produce large or consistent N2-P3a components; the critical condition for the generation of an N2-P3a wave seemed to be that the infrequent sounds represent a deviation (intensity increment or decrement) from a repetitive background. Furthermore, increasing the repetition rate of the background clicks drastically reduced N1-P2 amplitude but had little effect on the amplitude of N2-P3a. This suggests that N2-P3a is not simply a delayed N1-P2 "vertex potential," but rather reflects the operation of a "mismatch" detector, which registers deviations from an ongoing auditory background.
When a subject attends to a train of repetitive auditory stimuli in order to detect an i n f r e q u e n t "target" stimulus such as a pitch change (Ritter et al., 1972), i n t e n s i t y sbdft (Ritter and Vaughan, 1969; P i c t o n and Hillyard, 1974), or o m i t t e d stimulus (Picton et al., 1974; P i c t o n and Hillyard, 1974) w i t h i n that train, the averaged evoked potential (EP) to the target stimuli selectively develops an e n h a n c e d late positive wave (P3 or P300). This P3 wave, peaking at a latency of 3 0 0 - 4 5 0 msec, has most generally been interpreted as a neural correlate o f decision m a k i n g or signal d e t e c t i o n by an actively attending subject (Hillyard, 1969; Smith et al., 1970; Hillyard et al., 1971; Paul and S u t t o n , 1972). On the other hand, several authors (Ritter et al., 1968; R o t h , 1973; R o t h and Kopell, 1973; R o t h et al., 1973) have reported that a " P 3 " 1This work was supported by NIH Grant MH-25594-01 to S. A. Hillyard and NASA Grant NGR 05-009-198 to R. Galambos and was conducted while E. Snyder held a Sloan Foundation Fellowship. Address reprint requests to Elaine Snyder, Department of Neuroscience (A-012), University of California, San Diego, La Jolla, California 92093. 319 Copyright © 1976 by Academic Press, Inc. All rights of reproduction in any form reserved.
320
SNYDER AND HILLYARD
wave can also occur to infrequent, unpredictable stimulus changes under conditions where the subject is instructed to ignore the stimuli altogether. In an attempt to resolve this apparent inconsistency m the P3 literature, Squires, Squires, and Hillyard (1975) presented evidence that two distinct varieties of P3 waves (tentatively labeled "P3a" and "P3b") can be elicited depending on the circumstances. The "P3a" wave was evoked by "deviant" stimuli (pitch or intensity shifts) within a train of "standard" tone pips, whether they were being attended or not: this wave occurred earlier than the "classic" 300 msec (mean latency 265 msec) and had a fronto-central scalp distribution. In contrast, the P3b component was evoked only when the subject attended to the train of stimuli and performed some kind of response to the "deviant" stimuli (e.g., counted them). Moreover, the P3b wave had a scalp distribution with a parieto-central maximum amplitude and a mean latency of around 250 msec. The P3b seems to correspond in latency and topography to the "P3" reported in most prior studies (e.g., Ritter et al., 1972; Hillyard et al., 1976), while a late wave resembling the P3a appears in reports from Roth's laboratory (e.g., Roth, 1973). The identification of two varieties of late positive "P3" waves has helped to clarify some of the discrepancies in the literature but the nature of the P3a wave itself is little understood. Squires et al. (1975) noted that the P3a could be elicited by several types of deviant stimuli in an ongoing tram and suggested that P3a indexes a "mismatch" detection or "a basic sensory mechanism which registers any change in a background stimulus." Other interpretations still remain tenable, however. First, it may be that P3a represents activity of a neuronal population with a long refractory period that is specifically activated by the infrequent stimulus, whether or not it occurs by itself or as a deviation from an ongoing train. Because of its long refractory period, a P3a would not be evoked by the more frequent stimuli in the train. Squires et al. (1975) considered this interpretation unlikely since a rare intensity decrement in a train which elicited a large P3a would not be likely to activate a nonrefractory neural population separate from the one activated by the louder repetitive stimulus. Nonetheless, present evidence does not definitely rule out this possibility. A second hypothesis to be considered is that the P3a does not represent neural activity specific to a rare or deviant stimulus, but rather has a neural generator in common with the earlier P2 component of the auditory vertex potential; in this case, the deviant stimulus must act to delay the P2 by some 60-80 msec from its normal latency of 160-180 msec. In this connection, Squires et al. (1975) noted that the P3a was frequently preceded by an "N2" component at 180-200 msec, which might then represent a delayed Nl wave of the vertex potential. The present experiment was designed to explore these alternative interpretations of the recently-identified P3a component. To determine if P3a is simply a stimulus-specific component with a long refractory period,
EVOKED POTENTIALS TO IRRELEVANT, DEVIANT STIMULI
321
auditory EPs were compared when infrequent stimuli (clicks) were presented alone, as opposed to being embedded in repetitive trains of clicks of a different intensity. To find out whether the P3a generator can be dissociated from that of P2, the repetition rate of the ongoing train was manipulated, a procedure well known to influence P2 amplitude (Davis et al., 1966; Nelson and Lassman, 1968). If P3a reflects a straightforward mismatch detection operation, however, it might be expected to be relatively insensitive to stimulus repetition rate and thus dissociable from P2.
METHOD Subjects Twelve normal young adults (18-32 yr; 10 male and 2 female) served as subjects. Six of the subjects were naive as to the purpose of the experiment, four were laboratory personnel, and two were the authors. Stimuli The stimuli consisted of binaural clicks generated by passing 100/~sec square waves through earphones; the clicks were either "loud" (65 db SL) or "soft" (55 db SL) in intensity. Two basic types of stimulus sequences were used. In the first, clicks were given regularly at a fixed rate of 1/sec, 2/sec, or 3/sec in different blocks of the experiment; each block lasted five minutes. Within each block, 90% of the clicks were of one intensity (designated the "standard") while the remaining 10% were of the other intensity (designated the "rare" stimulus, which was interspersed at random in the sequence). Each block of trials contained a total of 32 rare stimuli. In the second type of stimulus sequence, the 32 rare stimuli were presented alone, at interstimulus intervals that were identical to those when the intervening standard stimuli were present. In all there were eight types of stimulus sequences: six with repetitive trains of stimuli (having loud and soft intensities as rare stimuli at each of three repetition rates), and two with rare stimuli presented alone (loud and soft stimuli). Procedure The subject was seated in a reclining chair and was instructed to minimize eye movements and blinks throughout the periods of stimulation. The eight stimulus sequences were administered in separate blocks with the subject reading a book under instructions to ignore the clicks ("inattend" condition). An additional two blocks of stimuli were given at the 1/sec rate while the subject counted the number of rare clicks within each block ("attend" condition); one of these sequences used soft rare clicks, the other
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