PS'yCHGPHYSIOl.OGY
Copyright ^ 1976 by The Society for Psychophysiologica! Research
Average Evoked Potential Changes as a Function of Processing Complexity LEONARD W . POON, LARRY W . THOMPSON, AND GAIL R. MARSH Duke University Medical Center and The Center for the Study of Aging and Human Development
ABSTRACT Electrophysiologic potentials (average evoked potentials (AEP) and contingent negative variation (CNV)) recorded during simple recognition and discriminative responses to tachistoscopically presented letter-pair stimuli showed a systematic shift toward greater overall positivity (i.e., smaller CNVs and larger late positive components) during increased processing load. In addition, more positive P2 components were found in the right as compared to the left hemisphere during simple recognition, and this asymmetry was enhanced during the more complex processing condition. DESCRIPTORS: Average evoked potential. Information processing. Reaction time. Cerebral asymmetry. Average evoked potentials (AEPs) recorded from the human scalp have been found to reliably reflect changes in complex behavioral processes. For example, a slow negative-shift component of the AEP recorded in the period between a warning stimulus (Si) and an imperative stimulus (S2) and commonly known as the contingent negative variation (CNV) is found to positively associate with attentional variables (see Tecce, 1972, for review). A late positive component (LPC) of the AEP, measured 200-500 msec after stimulus onset, has been found to relate to selective attention, stimulus novelty, amount of information carried by the stimulus and the probability of its occurrence (see Sutton, 1969, and Karlin, 1970, for reviews). Recent studies have found relationships between aspects of the AEP and more complex behavior such as pattern learning (Donchin, Kubovy, Kutas, .Johnson, & Herning, 1973; Poon, Thompson, Williams, & Marsh, 1974) and discrimination problem-solving (Wilson, Harter, & Wells, 1973). The purpose of this study is to evaluate systematic changes in AEP between two levels of information processing by utilizing a modified version of a This investigation was supported in part by NIH Training GrantHD-00164 and in part by Research Grant HD-00668 from ihe National In.stitute of Child Health and Human DevelopmenS. The authors wish to thank Kathy Seiple for her aid in the cxillection and analysis of the data. The Second author is now at the Andrus Gerontology Center, tJniversity of Southern California. Los Angeles, CA 90007. Address requests for reprints to: Leonard W. Poon, Ph.D., who is now at Normative Aging Study, VA Outpatient Clinic, 2.S Huntington Ave. (Rm. 322), Boston, MA 02116.
procedure employed by Posner and Mitchell (1967). Posner and Mitchell used a "same-different" reaction time task to study processing latencies for different levels of difficulty of perceptual matching and classification. The stimuli were always pairs of letters and the subjects were required to make decisions about "physical identity," "name identit y , " or "rule identity." The present study evaluated changes in AEP between information processed at a relatively easy recognition level and a more difficult complex rule classification level. Perceptual asymmetry between the hemispheres has been reported using the Posner and Mitchell procedure. Geffen, Bradshaw, andNettleton (1972) found faster responses to the name identity task when letters were presented to the left hemisphere, and faster responses to the physical identity task when the letters were presented to the right hemisphere. The data were interpreted as support for the concept of hemispheric specialization in man. That is, the left hemisphere tends to show a superiority for verbal and language processes, while the right hemisphere tends to show a superiority for temporal and spatial processes. However, Gazzaniga (1970) has reported only partial support for Geffen et al. He described the same finding for the name identity task but found no difference in hemispheric lateralization for the physical identity task. As a second purpose of the present study, the concept of hemispheric lateralization was tested by comparing the AEP from left and right hemispheres recorded during simple recognition and verbal classification of letter stimuli. 43
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Vol. 13, No. I
POON, THOMPSON, AND MARSH Method Subjects
Nineteen Duke University students (ages 18 to 33) were paid $3!00 each for their participation iti this 1-hr experiment. All subjects were right-handed as determined by the Harris Test of Lateral Dominance (1947) and all had normal or corrected-tonormal vision. Procedure The subjects were told that they were to make decisions about pairs of letters projected tachistoscopically on a screen 2.25 m in front of them in an area 55 mm high x 55 mm wide (1,40 x 1.40 degrees of visual angle) centered on a fixation point. A red warning light (S,) located at the fixation point was illuminated for 1.4 sec preceding the presentation of the letters (S^). The mean intertrial interval was 17 sec with a range of 10-25 sec. Two different tasks were giveri to the subjects^a simple reaction time task (SRT) and a vowel-consonant (VC) task. In the SRT task, the subjects were in,structed to press a key as soon as they saw the letters. In the VC task, they were instructed to press one of two keys to indicate whether the two letters were both vowels or both consonants ("same") or whether the letter pair contained a vowel and a consonant ("different''). For both tasks, the subjects were instructed to make their re,sponses as fast as they could while still maintaining high accuracy. Identical letter pair stimuli were u,sed for both tasks but with a different presentation order. The order of task presentation was counterbalanced, and 32 trials were presented in each task. Postexperimental interviews were conducted to obtain the subjects' evaluation of task diificuity, amount of perceived anxiety, and amount of attention expended relative to each task. Apparatus and EEG Recording Presentation and timing of Sj and Sj were programmed by BRS/LVE digital logic controlling a Kodak Carousel 860 projector coupled with a Gerbrands electronic tachistoscopic shutter. Stimulus presentation duration was 100 msec. Reaction time was recorded to the nearest 0.1 msec on a Monsanto;model i OOA digital timer. EEGs were recorded with Beckman siiver/silver-chloride electrodes placed down the midline scalp at frontal (Fj), vertex (C^), and parietal (P,,) sites, and bilaterally over the temporal region (T, arid T4), according to the International 10-2(3 system. All electrode placements were referenced to linked right and left mastoids. Inter-electrode impedance (measured at lOHz) was kept below 2000 ohms and the epidermis was pricked with a sterile needle to eliminate any interference from skin generated artifacts (Picton & Hillyard, 1972). The electrodes were connected to Grass Pi7 DC high impedance amplifiers, which fed into Grass 7P1 low level DC preamplifiers modified to provide an 8 sec time constant and with a sensitivity setting of iOO(.iV/cm. Eye movemeBts were monitored by silver disc electrodes taped above the innerand below the outer canthus of the left eye. The electrodes were connected to a Grass 7P511 EEG amplifier (.sensitivity setting of 500 ^V/cm) with the low frequency filter set at 100 Hz, . EEGs were recorded by a Hewlett Packard 3955D FM tape recorder for off-line analysis. The EEG tracings during each trial were digitized from the tape recorded signals at 50 samples per sec by means df a Redcror A/D converter interfaced with an IBM i 130 computer. Four AEP components were measured: 1) the amplitude of the CNV was measured as the difference between
the mean value of a 600 msec baseline of EEG activity preceding S, and the mean of 200 njsec of CNV activity preceding Sj, 2) a negative component (Nl) measured from the pre-Si baseline to the maximum negative deflection 80-120 msec after Sj, 3) a positive component (P2) measured as the difference between the pre-Si baseline and the maximum positive deflection 180—220 msec after S2, 4) a positive component (P3) measured as the difference between the pre-Si baseline and the maximum positive deflection 280-400 msec after Sj. The measurements are illustrated in Fig. 1.
Results Significantly longer processing time was recorded for the VC task (average RT=1128 msec) compared to the SRT task (average RT==221 msec). The polygraph record was used for identification and for elimination of trials showing eye movement or other artifacts 2 sec before or after presentation of 82, A mean of 19 and 17 trials were retained for CNV averaging for the SRT and VC tasks respectively. Editing trials for movement artifacts yielded insufficient trials to obtain reliable CNVs (too many pre-Sj artifacts) for 2 subjects, and reliable LPCs (too many post-Sg artifacts) for 6 subjects. In addition, due to amplifier malfunction the gain for one of the temporal leads was too low for proper AEP averaging for 2 additional subjects. These data were dropped from subsequent analyses. In summary, trials entered for AEP averaging were free from artifacts; data from 17 subjects were used to evaluate CNV amplitude in the F^, C^, and ¥^ leads, and 14 subjects were used for the T3 and T4 leads. To evaluate the components N1, P2, and P3, in the Fj, C,,, and P^ leads 13 subjects were used, and for the T3 and T4 leads 11 subjects were used, Multivariate analyses of variance (MANOVA) (Jones, 1966) were employed, using a rejection region of/?^,05, to evaluate the systematic changes for each AEP component between the two tasks. Fig, 2 presents the mean AEP components measured antero-posteriorly for the two tasks. The figure shows that the VC task tends to produce more "positive" AEPs than the SRT task. That is, the VC task has both smaller CNV and N1 magnitudes, and larger P2 and P3 magnitudes, A specific, preplanned set of comparisons between tasks showed a significant task difference in amplitude
Fig, 1, An example of the scoring system used to analyze the AEP. This AEP was recorded from C,, during the VC task and represents 30 trials.
January, 1976
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TASK EFFECTS ON AEP AMPLITUDE
Pig. 3. Mean AEP components for the VC and SRT tasks measured at the left (T3) and right (T4) temporal sites.
found during the VC task for the Nl (F(!/ 10)=4.46) and P2 (F(1/1O)=68.36) components. Only the P2 component showed a significant difference between T3 and T4 (F(l/10)=9.82) during the SRT task. Discussion
Fig. 2. Mean AEP components for the VC and SRT tasks measured down the midSine at tVontal (F^), central (Cz), and parieta! (P,) sites.
between VC and SRT tasks for the CNV (F(3/ 14) = 5.57), Nl (F(3/10)=4.14), and P2 (F(3/ 10)=4.79) components. No significant task eifect was obtained for the P3 comp(went. The topographical distribution of the significant effects showed a significant task effect obtained at Q (F(l/16)==6.76) for the CNV component, at Q(F(l/12)=-6.85) for the N1 component, and at F^ (F(I/J2)=8.44) for the P2 component. These results imply the several interactions apparent in Fig. 2. Inspecting the task by recording sites' interaction in Fig. 2 showed a significant interaction for the C^-Pz site difference (F(l/ 16)= 15.68) for the CNV component. For the P2 component a significant interaction was found at the F^-P^ sites(F(l/12)=n.29). Fig. 3 presents the rqean AEP components tneasured at T3 and T4. Again, the VC task tends to be more "positive" than the SRT task. Asignificant task difference was obtained for the P2 (F(l/ ]Q)=5.26) and P3 (F( 1/10) =13.46) components. Fig. 3 also denotes the amount of asymmetry nieasured between the two electrode placements. Significant differences between T3 and T4 were
The five-fold increase in reaction time for the VC task denotes the increased complexity of the "rule identity" task beyond the simple recognition task. The AEPs show changes correlated with the increased latencies both before (i.e., CNV) and after (i.e., Nl, P2, P3) the presentation of the letter pair. First, the higher level of processing produced the more "positive" AEPs. Secondly, AEPs measured from the left temporal region were more "negative" than those measured from the right. This difference tended to be greater during the VC task fortheLPC. ,\ The most striking result of this study is the apparent shift toward "positivity" during the VC task. Both Figs. 2 and 3 illustrate this tendency for smaller CNV and Ni amplitudes and greater P2 and P3 amplitudes during the VC task. This tendency is apparent in all recording sites (though reduced in Earlier experiments (Davis, 1964; Spong, Haider, & Lindsley, 1965; Donchin & Cohen, 1967; Naatanen, 1967; Ritter & Vaughan, 1969) have established that larger LPCs are elicited by critical stimuli in situations where discriminative decisions are required. Chapman and Bragdon (1964), in an experiment similai' in several respects to the present one, demonstrated that stimuli which include material requiring cognitive processing elicited larger visual AEP late components than: those that did not, despite the fact that the blarik (no infonnation) stimuli were brighter and interspersed
46
POON, THOMPSON. AND MARSH
between the information carrying stimuli (see also Chapman, 1969). Greater LPCs have also been found in a pattern learning experiment during the acquisition period, when cognitive activity was greatest, and smaller LPCs obtained in an overlearning period when the correct response was wellleamed (Poon et al., 1974). This same study also found CNVs smaller during a learning task than during a straightforward reaction time task. Delse, Marsh, and Thompson (1972) have likewise found that smaller CNVs are associated with the more difficult discriminations in a tone discrimination task. Similarly, Roth, Kopell, Tinklenberg, Darley, Sikora, and Vesecky (in press) have found a smaller CNV during a more difficult short term memory problem. In short, the data from the present study seem to be congruent with those in the literature with respect to the association of a smaller CNV and a larger LPC with increased cognitive processing demands. The depression of negative-going and enhancement of positive-going activity for the VC task could be an indication that during the more cogriitively demanding task the average '' baseline'' of DC activity is closer to the physiological maxiihum for negativity. Negative-going components, therefore, have a more difficult time achieving the necessary physiologic conditions for expression, whereas the positive-going components find an environment more easily driven in that direction . Such a "ceiling effect'' has previously been hypothesized by Knott and Trwin (!967) in an attempt to explain why highly anxious subjects, who were likely to remain more aroused throughout all phases of their experiment, showed less CNV responsiveness to the experimental manipulation which attempted to increase CNV amplitudes. Donchia, Tueting, Ritter, Kutos, and Heffley (in press) have presented a similar conclusion. Effects of a similar nature can also be produced by specific experimental conditions. In a previous experiment, searching for an asymmetry in CNV between the hemispheres, the administration of verbal or nonverbal trials by blocks compared with administration of trials by random interspersion supported the concept of long-maintained baseline shifts throughout a block of trials (Marsh & Thompson, Note 1). In that report, when verbal or nonverbal trials were delivered by blocks no hemispheric asymmetries of CNV amplitude were shown. However with random interspersion of verbal and nonverbal trials CNV asymmetries did appear. This suggests that a tonically maintained shift is possible in the administration by block method, but that with a randomly interspersed trials method a CNV can only develop after Si is given when the appropriate expectancy is being adopted.
Vol. 1.1, No. I
In postexperimental interviews the subjects reported that they were more tense and anxious and that they had to use more concentration for the VC task. Unanimously, all subjects agreed that the VC task was more difficult. Thus a long-sustained baseline shift of DC activity during the VC task seems a reasonable hypothesis to explain the obtained data. When comparing the SRT and VC tasks, it could be argued that the shorter RT seen with decreasing rule complexity could lead to a motor component (i.e., a slight negativity before key pre.ss, a sharp negative wave at the time of key press, and a sharp positive wave following key press) being added to the CNV and AEP in the SRT task. Against this argument is the fact that no major changes in wave form were seen, although amplitude changes were characteristic. Such a wave form added to the AEP should have increased the amplitude of both negative and positive components, not the negative components alone. Also, the motor influence should be greatest near vertex and negligible over the temporal lobe, which runs counter to the present data. Finally, Ritter, Simpson, and Vaughan (1972) have shown that small motor movements as used in the present study do not produce motor components large enough to distort the wave forms of interest. Donchin et al. (1973) and Donchin et al. (in press) have shown that at vertex the requirement of a speedy response may suppress the effect of increasing processing complexity. So far no explanation of this suppression has been offered, but again for the reason stated above the motor component would seem a poor candidate for causing this effect. Also, in regard to contamination of the LPC by other electrocortica! phenomena, the question could be raised that differential CNV amplitudes in the two conditions could bias the ensuing LPC data. The results of Donchin et al. (in press) should dispel such doubts since they show that the amplitude of the LPC was unaffected by the addition of a warning signal and a factorial analysis demonstrated the CNV and LPC orthogonal. A recent experiment by Seales (1973) was theoretically and procedurally similar to ours. Employing 10 right-handed subjects, comparable reaction times were recorded: 300-310 for a simple task and 875-1100 for more complex tasks. He produced no asymmetry in AEP between O, and O2 or between a left and right "Wernicke area" placement for any of his tasks. He did, however, find differences in AEP components between a condition like our SRT task and two increasingly complex processing conditions (a "case (size) identity" and a "name identity"). From all of the above scalp areas he measured an early positive component (110-120 msec); an early negative
January, 1976
TASK EFFECTS ON AEP AMPLITUDE
(160-170 msec); a second large positive peak (280-380 msec); and a long latency, long duration, negative component (500-750 msec). Some differences between the simple and the more complex processing tasks were found. In general the more complex tasks delayed the onset, broadened and diminished the amplitude of the positive component at 280-380 msec, and considerably delayed the onset of the peak at 500-750 msec. These same changes could not be reliably produced at Q , however. Since none of the electrode locations used in the present experiment, except Cz, duplicate Seales' placements, direct comparison is difficult. In general, however, our results indicate an increase in positivity in the 280-380 msec period rather than a decrease. But a more imposing technical difference separates these two studies: Seales used a 0.12 sec time constant while our data was recorded essentially DC (8 sec time constant). Thus some of the slow potentials found in the present study would never have appeared under Seales' recording conditions. Unfortunately, such a difference in method is difficult to overcome and no attempt has been made to reanalyze the present data using a faster time constant. However, since Seales did not differentiate between the two positive components P2 and P3, the present data were reanalyzed using a "most positive point" criterion to evaluate compatibility between the studies. This reanalysis of our data led, in general, to results very similar to those obtained for the P2 component. The differences between the studies remain for further investigation. Another aspect of the present results of some interest is that the F^ and C^ recording sites showed far more differences between conditions than did P,,. That the greatest difference between conditions would be seen at Fz was unexpected since Vaughan and Ritter (1970) had shown that the P3 component of the auditory AEP was generated largely from the parietal cortex. Nonetheless it seems clear that both the P2 and P3 components show significant differences between simple and complex tasks only at F?. This observation has a bearing upon Pribram's (1969, 1970) model of the functioning of the intrinsic cortex. Briefly, the model conceptualized the frontal cortex as concemed wiith mechanisms of vigilance such as monitoring for significant events, while the posterior cortex was seen as an integrator of information. An evaluation of this model using CNV as an indicator of the area of cortical involvement was attempted by Poon et al. (1974) employing a sequential pattern-learning task, in which the subject had to focus on the integralioni of trial-by-trial information, and also a disjunctive RT task, in which the subject was to react to one color of
47
a signal light and not to another. The parietal area was found to have the greatest CNV amplitude during the pattern-learning task while the vertex was found to have the greatest amplitude during the RT task. The result was interpreted as partial support for that aspect of Pribram's model which suggests that the posterior area of the cortex is involved in the integration of information. Although the dominant CNV shifted forward to the vertex for the RT task, the result did not support the hypothesis that the frontal cortex (i.e., F^) was responsible for vigilance and monitoring functions. While the present procedure required the subject to make discrete decisions, no integration of trial-bytrial information was needed. This may have led to the finding of no difference between the conditions for either the P2 or P3 components at the parietal area. But the finding of greater P2 and P3 components in the frontal area during the VC task would seem contrary to the hypothesized function of monitoring for significant events. A recent report has found the frontal area producing differential AEPs to identical stimuli when given different names while the occipital scalp did not (Johnson & Chesney, 1974). Perhaps the present differential results for the frontal area would be best characterized as LPC changes due to increased verbal processing and not to increased monitoring or vigilance demands. Conflicting results have been reported in regard to AEP asymmetry. Marsh and Thompson (Note 1) found greater CNV amplitude in the right temporal region for verbal stimuli and greater CNV in the left parietal region for spatial stimuli. Contrary to this finding, Butler and Glass (1971) found larger CNV over the left hemisphere during a mental arithmetic task which presumably engaged the left hemisphere. In the present experiment, CNVs tended to be larger in the left temporal areas during the SRT task and even more asymmetric during the VC task. However, none of these trends reached statistical significance. Hemispheric asymmetry for the AEP has been studied using auditory stimuli to contrast verbal and nonverbal stimuli (MoiTeil & Salamy, 1971; Wood, Goff, & Day, 1971; Molfese, 1972). Although cognitive aspects of the stimuli in these studies were not emphasized, a larger amplitude negative component 100-200 msec after the stimulus was found in the left hemisphere. A similar finding was observed for the N1 component for the VC task in this experiment. Matsumiya, Tagliasco, Lombroso, and Goodglass (1972) did emphasize tlic cognitive aspects of their study with auditory AEP. They found an asymmetry in the 100-200 msec latency range and reported a \atgt positive component in the left hemisphere.
48
POON. THOMPSON. AND MARSH
Studies examining LPC asymmetry in the visual modality have often relied on simple flash stimuli in noncognitive test situations (Rhodes, Dustman, & Beck, 1969; Bigum, Dustman, & Beck, 1970; Lewis, Dustman, & Beck, 1970; Schenkenberg, 1970; Schenkenberg & Dustman, 1970; Richlin, Weisinger, Weinstein, Giannini, & Morganstern, 1971). Furthermore, larger amplitude AEPs have been found in the right temporo-parietal region in high IQ, but not low IQ subjects. Buchsbaum and Fedio (1969, 1970) used verbal and spatial stimuli, but with an unusual method of measuring the AEP, which did not permit direct amplitude measurements. However, they did report that the left hemi.sphere showed greater changes between the two types of stimuli than did the right. Seales (1973)
Vol. 13. No. I
found no AEP asymmetry in any of the task conditions or in either of the two homologous sites which were compared in that study. The discrepancy between the results of the Seales study and the present one could be due to technical differences already mentioned. A more positive P2 was found in the right hemisphere during the SRT task in this experiment. Since this asymmetry was enhanced rather than reversed for the VC task, it is possible that, in their boredom, the subjects attended to the letter stimuli as verbal symbols during the SRT task, making this a verbal task, and that the enhanced asymmetry during the VC task reflected a greater degree of verbal processing.
REFERENCES Bigum. H. B,. Dustman, R. E.. & Beck. E. C. Visual and somatosensory evoked re.sponscs from mongoloid and normal children. Electroencephalography & Clinical Neurophysiology, 1970, 2H, 576-585. Buchsbaum, M.. & Fedio. P. Visual information and evoked responses from the left and right hemispheres. Eleciroenvephalography & Clinical Neurophysiology, 1969, 26, 266-272. Buchsbaiim, M., & Fedio. P. Hemispheric differences in evoked potentials to verbal and nonverbal stimuli in the left and right visual ^eXda. Physiology & Behavior, 1970, 5, 207-210. Butler, S. R.. & Glass, A. Interhemispheric asymmetry of eontingent negative variation during numeric operations. Eiectroencephalography & Clinical Neurophysiology, 197), 30, 366. (Abstract) . Chapman, R. M. Oiscus.sion. In E. Donchin & D. B. Lindsley (Eds.), Average evoked potentials: Method.',, resulLs, and evaluations. (NASA SP-191) Washington, D . C : U.S. Government Printing Office, 1969. Pp. 262-275. Ghapnian, R. M., & Bragdon, H. R. Evoked respon.ses to : numerical and non-numerieal visual stimuli while problem solving. A'aw?-^', 1964, 20J, l ! 5 5 - n 5 7 . Davis, H, Enhancement of evoked cortical potentials in humans related to a task requiring a decision. Science, 1964, /45, !82-183. Delse. F. C M i i r s h , G. R., & Thompson, L. W, CNV correlates of task difficulty and accuracy of pitch discrimination. Fsychaphy.siology, 1^/72, 9, 53-62. D
Copyright ^ 1976 by The Society for Psychophysiologica! Research
Average Evoked Potential Changes as a Function of Processing Complexity LEONARD W . POON, LARRY W . THOMPSON, AND GAIL R. MARSH Duke University Medical Center and The Center for the Study of Aging and Human Development
ABSTRACT Electrophysiologic potentials (average evoked potentials (AEP) and contingent negative variation (CNV)) recorded during simple recognition and discriminative responses to tachistoscopically presented letter-pair stimuli showed a systematic shift toward greater overall positivity (i.e., smaller CNVs and larger late positive components) during increased processing load. In addition, more positive P2 components were found in the right as compared to the left hemisphere during simple recognition, and this asymmetry was enhanced during the more complex processing condition. DESCRIPTORS: Average evoked potential. Information processing. Reaction time. Cerebral asymmetry. Average evoked potentials (AEPs) recorded from the human scalp have been found to reliably reflect changes in complex behavioral processes. For example, a slow negative-shift component of the AEP recorded in the period between a warning stimulus (Si) and an imperative stimulus (S2) and commonly known as the contingent negative variation (CNV) is found to positively associate with attentional variables (see Tecce, 1972, for review). A late positive component (LPC) of the AEP, measured 200-500 msec after stimulus onset, has been found to relate to selective attention, stimulus novelty, amount of information carried by the stimulus and the probability of its occurrence (see Sutton, 1969, and Karlin, 1970, for reviews). Recent studies have found relationships between aspects of the AEP and more complex behavior such as pattern learning (Donchin, Kubovy, Kutas, .Johnson, & Herning, 1973; Poon, Thompson, Williams, & Marsh, 1974) and discrimination problem-solving (Wilson, Harter, & Wells, 1973). The purpose of this study is to evaluate systematic changes in AEP between two levels of information processing by utilizing a modified version of a This investigation was supported in part by NIH Training GrantHD-00164 and in part by Research Grant HD-00668 from ihe National In.stitute of Child Health and Human DevelopmenS. The authors wish to thank Kathy Seiple for her aid in the cxillection and analysis of the data. The Second author is now at the Andrus Gerontology Center, tJniversity of Southern California. Los Angeles, CA 90007. Address requests for reprints to: Leonard W. Poon, Ph.D., who is now at Normative Aging Study, VA Outpatient Clinic, 2.S Huntington Ave. (Rm. 322), Boston, MA 02116.
procedure employed by Posner and Mitchell (1967). Posner and Mitchell used a "same-different" reaction time task to study processing latencies for different levels of difficulty of perceptual matching and classification. The stimuli were always pairs of letters and the subjects were required to make decisions about "physical identity," "name identit y , " or "rule identity." The present study evaluated changes in AEP between information processed at a relatively easy recognition level and a more difficult complex rule classification level. Perceptual asymmetry between the hemispheres has been reported using the Posner and Mitchell procedure. Geffen, Bradshaw, andNettleton (1972) found faster responses to the name identity task when letters were presented to the left hemisphere, and faster responses to the physical identity task when the letters were presented to the right hemisphere. The data were interpreted as support for the concept of hemispheric specialization in man. That is, the left hemisphere tends to show a superiority for verbal and language processes, while the right hemisphere tends to show a superiority for temporal and spatial processes. However, Gazzaniga (1970) has reported only partial support for Geffen et al. He described the same finding for the name identity task but found no difference in hemispheric lateralization for the physical identity task. As a second purpose of the present study, the concept of hemispheric lateralization was tested by comparing the AEP from left and right hemispheres recorded during simple recognition and verbal classification of letter stimuli. 43
44
Vol. 13, No. I
POON, THOMPSON, AND MARSH Method Subjects
Nineteen Duke University students (ages 18 to 33) were paid $3!00 each for their participation iti this 1-hr experiment. All subjects were right-handed as determined by the Harris Test of Lateral Dominance (1947) and all had normal or corrected-tonormal vision. Procedure The subjects were told that they were to make decisions about pairs of letters projected tachistoscopically on a screen 2.25 m in front of them in an area 55 mm high x 55 mm wide (1,40 x 1.40 degrees of visual angle) centered on a fixation point. A red warning light (S,) located at the fixation point was illuminated for 1.4 sec preceding the presentation of the letters (S^). The mean intertrial interval was 17 sec with a range of 10-25 sec. Two different tasks were giveri to the subjects^a simple reaction time task (SRT) and a vowel-consonant (VC) task. In the SRT task, the subjects were in,structed to press a key as soon as they saw the letters. In the VC task, they were instructed to press one of two keys to indicate whether the two letters were both vowels or both consonants ("same") or whether the letter pair contained a vowel and a consonant ("different''). For both tasks, the subjects were instructed to make their re,sponses as fast as they could while still maintaining high accuracy. Identical letter pair stimuli were u,sed for both tasks but with a different presentation order. The order of task presentation was counterbalanced, and 32 trials were presented in each task. Postexperimental interviews were conducted to obtain the subjects' evaluation of task diificuity, amount of perceived anxiety, and amount of attention expended relative to each task. Apparatus and EEG Recording Presentation and timing of Sj and Sj were programmed by BRS/LVE digital logic controlling a Kodak Carousel 860 projector coupled with a Gerbrands electronic tachistoscopic shutter. Stimulus presentation duration was 100 msec. Reaction time was recorded to the nearest 0.1 msec on a Monsanto;model i OOA digital timer. EEGs were recorded with Beckman siiver/silver-chloride electrodes placed down the midline scalp at frontal (Fj), vertex (C^), and parietal (P,,) sites, and bilaterally over the temporal region (T, arid T4), according to the International 10-2(3 system. All electrode placements were referenced to linked right and left mastoids. Inter-electrode impedance (measured at lOHz) was kept below 2000 ohms and the epidermis was pricked with a sterile needle to eliminate any interference from skin generated artifacts (Picton & Hillyard, 1972). The electrodes were connected to Grass Pi7 DC high impedance amplifiers, which fed into Grass 7P1 low level DC preamplifiers modified to provide an 8 sec time constant and with a sensitivity setting of iOO(.iV/cm. Eye movemeBts were monitored by silver disc electrodes taped above the innerand below the outer canthus of the left eye. The electrodes were connected to a Grass 7P511 EEG amplifier (.sensitivity setting of 500 ^V/cm) with the low frequency filter set at 100 Hz, . EEGs were recorded by a Hewlett Packard 3955D FM tape recorder for off-line analysis. The EEG tracings during each trial were digitized from the tape recorded signals at 50 samples per sec by means df a Redcror A/D converter interfaced with an IBM i 130 computer. Four AEP components were measured: 1) the amplitude of the CNV was measured as the difference between
the mean value of a 600 msec baseline of EEG activity preceding S, and the mean of 200 njsec of CNV activity preceding Sj, 2) a negative component (Nl) measured from the pre-Si baseline to the maximum negative deflection 80-120 msec after Sj, 3) a positive component (P2) measured as the difference between the pre-Si baseline and the maximum positive deflection 180—220 msec after S2, 4) a positive component (P3) measured as the difference between the pre-Si baseline and the maximum positive deflection 280-400 msec after Sj. The measurements are illustrated in Fig. 1.
Results Significantly longer processing time was recorded for the VC task (average RT=1128 msec) compared to the SRT task (average RT==221 msec). The polygraph record was used for identification and for elimination of trials showing eye movement or other artifacts 2 sec before or after presentation of 82, A mean of 19 and 17 trials were retained for CNV averaging for the SRT and VC tasks respectively. Editing trials for movement artifacts yielded insufficient trials to obtain reliable CNVs (too many pre-Sj artifacts) for 2 subjects, and reliable LPCs (too many post-Sg artifacts) for 6 subjects. In addition, due to amplifier malfunction the gain for one of the temporal leads was too low for proper AEP averaging for 2 additional subjects. These data were dropped from subsequent analyses. In summary, trials entered for AEP averaging were free from artifacts; data from 17 subjects were used to evaluate CNV amplitude in the F^, C^, and ¥^ leads, and 14 subjects were used for the T3 and T4 leads. To evaluate the components N1, P2, and P3, in the Fj, C,,, and P^ leads 13 subjects were used, and for the T3 and T4 leads 11 subjects were used, Multivariate analyses of variance (MANOVA) (Jones, 1966) were employed, using a rejection region of/?^,05, to evaluate the systematic changes for each AEP component between the two tasks. Fig, 2 presents the mean AEP components measured antero-posteriorly for the two tasks. The figure shows that the VC task tends to produce more "positive" AEPs than the SRT task. That is, the VC task has both smaller CNV and N1 magnitudes, and larger P2 and P3 magnitudes, A specific, preplanned set of comparisons between tasks showed a significant task difference in amplitude
Fig, 1, An example of the scoring system used to analyze the AEP. This AEP was recorded from C,, during the VC task and represents 30 trials.
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TASK EFFECTS ON AEP AMPLITUDE
Pig. 3. Mean AEP components for the VC and SRT tasks measured at the left (T3) and right (T4) temporal sites.
found during the VC task for the Nl (F(!/ 10)=4.46) and P2 (F(1/1O)=68.36) components. Only the P2 component showed a significant difference between T3 and T4 (F(l/10)=9.82) during the SRT task. Discussion
Fig. 2. Mean AEP components for the VC and SRT tasks measured down the midSine at tVontal (F^), central (Cz), and parieta! (P,) sites.
between VC and SRT tasks for the CNV (F(3/ 14) = 5.57), Nl (F(3/10)=4.14), and P2 (F(3/ 10)=4.79) components. No significant task eifect was obtained for the P3 comp(went. The topographical distribution of the significant effects showed a significant task effect obtained at Q (F(l/16)==6.76) for the CNV component, at Q(F(l/12)=-6.85) for the N1 component, and at F^ (F(I/J2)=8.44) for the P2 component. These results imply the several interactions apparent in Fig. 2. Inspecting the task by recording sites' interaction in Fig. 2 showed a significant interaction for the C^-Pz site difference (F(l/ 16)= 15.68) for the CNV component. For the P2 component a significant interaction was found at the F^-P^ sites(F(l/12)=n.29). Fig. 3 presents the rqean AEP components tneasured at T3 and T4. Again, the VC task tends to be more "positive" than the SRT task. Asignificant task difference was obtained for the P2 (F(l/ ]Q)=5.26) and P3 (F( 1/10) =13.46) components. Fig. 3 also denotes the amount of asymmetry nieasured between the two electrode placements. Significant differences between T3 and T4 were
The five-fold increase in reaction time for the VC task denotes the increased complexity of the "rule identity" task beyond the simple recognition task. The AEPs show changes correlated with the increased latencies both before (i.e., CNV) and after (i.e., Nl, P2, P3) the presentation of the letter pair. First, the higher level of processing produced the more "positive" AEPs. Secondly, AEPs measured from the left temporal region were more "negative" than those measured from the right. This difference tended to be greater during the VC task fortheLPC. ,\ The most striking result of this study is the apparent shift toward "positivity" during the VC task. Both Figs. 2 and 3 illustrate this tendency for smaller CNV and Ni amplitudes and greater P2 and P3 amplitudes during the VC task. This tendency is apparent in all recording sites (though reduced in Earlier experiments (Davis, 1964; Spong, Haider, & Lindsley, 1965; Donchin & Cohen, 1967; Naatanen, 1967; Ritter & Vaughan, 1969) have established that larger LPCs are elicited by critical stimuli in situations where discriminative decisions are required. Chapman and Bragdon (1964), in an experiment similai' in several respects to the present one, demonstrated that stimuli which include material requiring cognitive processing elicited larger visual AEP late components than: those that did not, despite the fact that the blarik (no infonnation) stimuli were brighter and interspersed
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between the information carrying stimuli (see also Chapman, 1969). Greater LPCs have also been found in a pattern learning experiment during the acquisition period, when cognitive activity was greatest, and smaller LPCs obtained in an overlearning period when the correct response was wellleamed (Poon et al., 1974). This same study also found CNVs smaller during a learning task than during a straightforward reaction time task. Delse, Marsh, and Thompson (1972) have likewise found that smaller CNVs are associated with the more difficult discriminations in a tone discrimination task. Similarly, Roth, Kopell, Tinklenberg, Darley, Sikora, and Vesecky (in press) have found a smaller CNV during a more difficult short term memory problem. In short, the data from the present study seem to be congruent with those in the literature with respect to the association of a smaller CNV and a larger LPC with increased cognitive processing demands. The depression of negative-going and enhancement of positive-going activity for the VC task could be an indication that during the more cogriitively demanding task the average '' baseline'' of DC activity is closer to the physiological maxiihum for negativity. Negative-going components, therefore, have a more difficult time achieving the necessary physiologic conditions for expression, whereas the positive-going components find an environment more easily driven in that direction . Such a "ceiling effect'' has previously been hypothesized by Knott and Trwin (!967) in an attempt to explain why highly anxious subjects, who were likely to remain more aroused throughout all phases of their experiment, showed less CNV responsiveness to the experimental manipulation which attempted to increase CNV amplitudes. Donchia, Tueting, Ritter, Kutos, and Heffley (in press) have presented a similar conclusion. Effects of a similar nature can also be produced by specific experimental conditions. In a previous experiment, searching for an asymmetry in CNV between the hemispheres, the administration of verbal or nonverbal trials by blocks compared with administration of trials by random interspersion supported the concept of long-maintained baseline shifts throughout a block of trials (Marsh & Thompson, Note 1). In that report, when verbal or nonverbal trials were delivered by blocks no hemispheric asymmetries of CNV amplitude were shown. However with random interspersion of verbal and nonverbal trials CNV asymmetries did appear. This suggests that a tonically maintained shift is possible in the administration by block method, but that with a randomly interspersed trials method a CNV can only develop after Si is given when the appropriate expectancy is being adopted.
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In postexperimental interviews the subjects reported that they were more tense and anxious and that they had to use more concentration for the VC task. Unanimously, all subjects agreed that the VC task was more difficult. Thus a long-sustained baseline shift of DC activity during the VC task seems a reasonable hypothesis to explain the obtained data. When comparing the SRT and VC tasks, it could be argued that the shorter RT seen with decreasing rule complexity could lead to a motor component (i.e., a slight negativity before key pre.ss, a sharp negative wave at the time of key press, and a sharp positive wave following key press) being added to the CNV and AEP in the SRT task. Against this argument is the fact that no major changes in wave form were seen, although amplitude changes were characteristic. Such a wave form added to the AEP should have increased the amplitude of both negative and positive components, not the negative components alone. Also, the motor influence should be greatest near vertex and negligible over the temporal lobe, which runs counter to the present data. Finally, Ritter, Simpson, and Vaughan (1972) have shown that small motor movements as used in the present study do not produce motor components large enough to distort the wave forms of interest. Donchin et al. (1973) and Donchin et al. (in press) have shown that at vertex the requirement of a speedy response may suppress the effect of increasing processing complexity. So far no explanation of this suppression has been offered, but again for the reason stated above the motor component would seem a poor candidate for causing this effect. Also, in regard to contamination of the LPC by other electrocortica! phenomena, the question could be raised that differential CNV amplitudes in the two conditions could bias the ensuing LPC data. The results of Donchin et al. (in press) should dispel such doubts since they show that the amplitude of the LPC was unaffected by the addition of a warning signal and a factorial analysis demonstrated the CNV and LPC orthogonal. A recent experiment by Seales (1973) was theoretically and procedurally similar to ours. Employing 10 right-handed subjects, comparable reaction times were recorded: 300-310 for a simple task and 875-1100 for more complex tasks. He produced no asymmetry in AEP between O, and O2 or between a left and right "Wernicke area" placement for any of his tasks. He did, however, find differences in AEP components between a condition like our SRT task and two increasingly complex processing conditions (a "case (size) identity" and a "name identity"). From all of the above scalp areas he measured an early positive component (110-120 msec); an early negative
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TASK EFFECTS ON AEP AMPLITUDE
(160-170 msec); a second large positive peak (280-380 msec); and a long latency, long duration, negative component (500-750 msec). Some differences between the simple and the more complex processing tasks were found. In general the more complex tasks delayed the onset, broadened and diminished the amplitude of the positive component at 280-380 msec, and considerably delayed the onset of the peak at 500-750 msec. These same changes could not be reliably produced at Q , however. Since none of the electrode locations used in the present experiment, except Cz, duplicate Seales' placements, direct comparison is difficult. In general, however, our results indicate an increase in positivity in the 280-380 msec period rather than a decrease. But a more imposing technical difference separates these two studies: Seales used a 0.12 sec time constant while our data was recorded essentially DC (8 sec time constant). Thus some of the slow potentials found in the present study would never have appeared under Seales' recording conditions. Unfortunately, such a difference in method is difficult to overcome and no attempt has been made to reanalyze the present data using a faster time constant. However, since Seales did not differentiate between the two positive components P2 and P3, the present data were reanalyzed using a "most positive point" criterion to evaluate compatibility between the studies. This reanalysis of our data led, in general, to results very similar to those obtained for the P2 component. The differences between the studies remain for further investigation. Another aspect of the present results of some interest is that the F^ and C^ recording sites showed far more differences between conditions than did P,,. That the greatest difference between conditions would be seen at Fz was unexpected since Vaughan and Ritter (1970) had shown that the P3 component of the auditory AEP was generated largely from the parietal cortex. Nonetheless it seems clear that both the P2 and P3 components show significant differences between simple and complex tasks only at F?. This observation has a bearing upon Pribram's (1969, 1970) model of the functioning of the intrinsic cortex. Briefly, the model conceptualized the frontal cortex as concemed wiith mechanisms of vigilance such as monitoring for significant events, while the posterior cortex was seen as an integrator of information. An evaluation of this model using CNV as an indicator of the area of cortical involvement was attempted by Poon et al. (1974) employing a sequential pattern-learning task, in which the subject had to focus on the integralioni of trial-by-trial information, and also a disjunctive RT task, in which the subject was to react to one color of
47
a signal light and not to another. The parietal area was found to have the greatest CNV amplitude during the pattern-learning task while the vertex was found to have the greatest amplitude during the RT task. The result was interpreted as partial support for that aspect of Pribram's model which suggests that the posterior area of the cortex is involved in the integration of information. Although the dominant CNV shifted forward to the vertex for the RT task, the result did not support the hypothesis that the frontal cortex (i.e., F^) was responsible for vigilance and monitoring functions. While the present procedure required the subject to make discrete decisions, no integration of trial-bytrial information was needed. This may have led to the finding of no difference between the conditions for either the P2 or P3 components at the parietal area. But the finding of greater P2 and P3 components in the frontal area during the VC task would seem contrary to the hypothesized function of monitoring for significant events. A recent report has found the frontal area producing differential AEPs to identical stimuli when given different names while the occipital scalp did not (Johnson & Chesney, 1974). Perhaps the present differential results for the frontal area would be best characterized as LPC changes due to increased verbal processing and not to increased monitoring or vigilance demands. Conflicting results have been reported in regard to AEP asymmetry. Marsh and Thompson (Note 1) found greater CNV amplitude in the right temporal region for verbal stimuli and greater CNV in the left parietal region for spatial stimuli. Contrary to this finding, Butler and Glass (1971) found larger CNV over the left hemisphere during a mental arithmetic task which presumably engaged the left hemisphere. In the present experiment, CNVs tended to be larger in the left temporal areas during the SRT task and even more asymmetric during the VC task. However, none of these trends reached statistical significance. Hemispheric asymmetry for the AEP has been studied using auditory stimuli to contrast verbal and nonverbal stimuli (MoiTeil & Salamy, 1971; Wood, Goff, & Day, 1971; Molfese, 1972). Although cognitive aspects of the stimuli in these studies were not emphasized, a larger amplitude negative component 100-200 msec after the stimulus was found in the left hemisphere. A similar finding was observed for the N1 component for the VC task in this experiment. Matsumiya, Tagliasco, Lombroso, and Goodglass (1972) did emphasize tlic cognitive aspects of their study with auditory AEP. They found an asymmetry in the 100-200 msec latency range and reported a \atgt positive component in the left hemisphere.
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Studies examining LPC asymmetry in the visual modality have often relied on simple flash stimuli in noncognitive test situations (Rhodes, Dustman, & Beck, 1969; Bigum, Dustman, & Beck, 1970; Lewis, Dustman, & Beck, 1970; Schenkenberg, 1970; Schenkenberg & Dustman, 1970; Richlin, Weisinger, Weinstein, Giannini, & Morganstern, 1971). Furthermore, larger amplitude AEPs have been found in the right temporo-parietal region in high IQ, but not low IQ subjects. Buchsbaum and Fedio (1969, 1970) used verbal and spatial stimuli, but with an unusual method of measuring the AEP, which did not permit direct amplitude measurements. However, they did report that the left hemi.sphere showed greater changes between the two types of stimuli than did the right. Seales (1973)
Vol. 13. No. I
found no AEP asymmetry in any of the task conditions or in either of the two homologous sites which were compared in that study. The discrepancy between the results of the Seales study and the present one could be due to technical differences already mentioned. A more positive P2 was found in the right hemisphere during the SRT task in this experiment. Since this asymmetry was enhanced rather than reversed for the VC task, it is possible that, in their boredom, the subjects attended to the letter stimuli as verbal symbols during the SRT task, making this a verbal task, and that the enhanced asymmetry during the VC task reflected a greater degree of verbal processing.
REFERENCES Bigum. H. B,. Dustman, R. E.. & Beck. E. C. Visual and somatosensory evoked re.sponscs from mongoloid and normal children. Electroencephalography & Clinical Neurophysiology, 1970, 2H, 576-585. Buchsbaum, M.. & Fedio. P. Visual information and evoked responses from the left and right hemispheres. Eleciroenvephalography & Clinical Neurophysiology, 1969, 26, 266-272. Buchsbaiim, M., & Fedio. P. Hemispheric differences in evoked potentials to verbal and nonverbal stimuli in the left and right visual ^eXda. Physiology & Behavior, 1970, 5, 207-210. Butler, S. R.. & Glass, A. Interhemispheric asymmetry of eontingent negative variation during numeric operations. Eiectroencephalography & Clinical Neurophysiology, 197), 30, 366. (Abstract) . Chapman, R. M. Oiscus.sion. In E. Donchin & D. B. Lindsley (Eds.), Average evoked potentials: Method.',, resulLs, and evaluations. (NASA SP-191) Washington, D . C : U.S. Government Printing Office, 1969. Pp. 262-275. Ghapnian, R. M., & Bragdon, H. R. Evoked respon.ses to : numerical and non-numerieal visual stimuli while problem solving. A'aw?-^', 1964, 20J, l ! 5 5 - n 5 7 . Davis, H, Enhancement of evoked cortical potentials in humans related to a task requiring a decision. Science, 1964, /45, !82-183. Delse. F. C M i i r s h , G. R., & Thompson, L. W, CNV correlates of task difficulty and accuracy of pitch discrimination. Fsychaphy.siology, 1^/72, 9, 53-62. D
