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Selective attention and “habituation” of the auditory averaged evoked response in humans
Physiology andBehavtor Vol. 8, pp. 79-85. Brain Research Publications, Inc., 1972. Printed in U.S.A.
Selective Attention and "Habituation" of the Auditory Averaged Evoked Response in Humans'" ARNE ()HMAN 3 AND MALCOLM L A D E R 4
Institute o f Psychiatry, University o f London, Denmark Hill, London S.E. 5, U..K.
(Received 6 July 1971) OHMAN, A. AND M. H. LADER. Selective attention and "habituation" of the auditory averaged evoked responl¢ in humans. PHYSIOL. BEHAV. 8 (1) 79-85, 1972.-The study examined the effects of dixeettoa of attention and interstimulus interval on the rate of amplitude decrement over time of the vertex auditory evoked response in hummu. Short-term or stimulus-by-stimulus changes were studied by averaging aczoss 24 disczetely pteNnted ttsim each of 10 click stimuli. Long-term or train-by-train changes were studied by averaging over successive pairs of traim. Wlum atteadhl$ to the clicks, the subject performed a reaction-time (RT) task with the crick as stimulus; when i p m ' i ~ the dic3~ he peffmmed RTs to a visual stimulus. Both RT tasks were performed with irregular inte~ttlmulu$ intervals of 2.4 - 3.6 and 8 - 12 s, each of the 8 subjects being thus studied on four occasions. Atteading to the stimuli and long iatent~ult~t iatervals enhanced the PI-Nt-P2 components. Amplitude decreased over time both for Jtimulus-by-~]mulu lead tmia-by.ttatn averages. Somewhat unexpectedly, there was a slight but significant tendency towards a steeper slope for the attending and long interstimulus interval conditions, probably following on the larger initial responses for these condiiiem. Auditory average evoked response
Response decrement over time
Habituation
Attention
lnter~timuhis interval
On a more theoretical level, the response decrement of the AER could have clear psychological correlates, tending to suggest a psychological mechan~m, o r it couJd be due to a more fundamental physiological mechanism such as neuronal recovery processes [20, 21 ; see also 3] . A putative psychological correlate is change in attention, or more specifically, distraction. Sokolov [ 2 3 ] , for example, suggested that the ork.lting responses to s t i m u l i t o which the subject attended habituated much more slowly than the responses to non-attended stimuli. Furthermore, Hernandez-Peon [l 2] and Walter [26] have implied that a similar relationship holds for the evoked potentials, i.e. one would expect the time course of response attenuation with repeated stimuli to differ according to whether attention directed toward or away from the stimuli. Thus, the effect of attention on AER amplitude [e.g. 2, 5, 8, 9, 10, I I , 17, 22, 24] could result from less respoose decrement in the attending than in the non-attending conditions, rather than from a direct effect of attention on response amplitucle. In the present study an a t t e m p t ]ms been made to delineate some o f the parameters controlling both shortand long-term changes in AER amplitude. Our main concern was with direction of attention, but since previous studies have indicated that interstimulus interval is another critical factor governing response attenuation [7, 20, 21],
IN SEVERAL recent studies of the averaged evoked response (AER) in humans, a drop in size o f the later potentials has been apparent as the stimuli were repeated, usually in the form of a slow, long-term change over several hundred stimulus presentations [8, 9, l l, 19]. Ritter et al. [20] introduced a method to study short-term or stimulus-by-stimulus changes by averaging across discretely presented trains o f stimuli, with an intertrain interval (ITI) of sufficient length to ensure complete recovery of the response between trains [cf. 3 ]. When a short interstimulus interval (ISI) was used, a very rapid decrement Over the.first few stimuli within a train was observed [7, 20, 21 ]. The inconstancy of the AER over stimulus presentations, with its systematic decreasing trend in amplitude, has important implications. F o r the averaging procedure to be justified, it must be assumed that the electroencephalographic activity that is time-locked to the stimulus remains fairly constant while the background EEG randomizes out. As the data seem to indicate that the time-locked activity does change with stimulus repetition, it is very important to elucidate the parameters which control these changes. Furthermore, any effect o f a variable on AER amplitude could be due either to a direct effect on response size or to an indirect effect on the rate of response decrement, since the AER by definition is derived from many trials.
2 Supported by the Medical Research Council of Great Britain. Requests for reprints should be addressed to M. Lader. 3Supported by a scholarship from the British Council and by travel grants from the Wallenb~g foundation. Present address: Department of Psychology, University of Uppsala, Svarth~'cksgatan I0, ,$-753 30 Uppmla, Sweden. 4Member of External Scientific Staff, Medical Research Council. 79
80
OHMAN AND LADER
this variable was also manipulated. In order to control for changes in general activation and performance, skin conductance level (SCL) and reaction-time (RT) were included as dependent variables. METHOD A total of 10 paid volunteer subjects, 3 females and 7 males (age range 22-33 years), including the authors, participated in the experiment. Two subjects were replaced after taking part in the first experimental condition because of small indistinct evoked responses, thus leaving complete data for 8 subjects. The subjects were members of the laboratory staff, and all but two had previously acted as subjects in experiments involving AER and reaction time. The subject was comfortably seated w i t h his eyes open and in a sound-protected room; the recording equipment was in an adjacent room. The experimental procedure was outlined and he was particularly instructed to avoid movements during the trains of stimuli. The experiment was performed on-line using a LINC-8 computer, which presented the stimuli, calculated and displayed reaction times (RTs), computed random ITIs and ISis, and sampled the EEG and skin resistance. The EEG was recorded from bipolar saline pad electrodes (Cz - T 3 on the 10-20 system) and fed through a Grass 511C amplifier of band-pass 0.3-1000 Hz to the A-D converter input of the LINC-8 computer. Skin conductance level (SCL) was recorded as resistance using double-element electrodes | 1 5 ] , the computer sampling the skin resistance immediately before each stimulus. The basic design was a 2 X 2 factorial, with attending vs. non-attending to auditory stimuli as one factor, and two different ISI's as the other. Thus, each subject was studied on four different occasions. The order of presentation of conditions was counterbalanced so that each condition preceded or followed all other conditions an equal n u m b e r of times. The between condition interval for a subject was at least 3 days. In all the conditions, auditory evoked responses were measured to clicks of about 70 db intensity and 1 ms in duration presented through a loudspeaker behind the subject. The stimuli appeared in trains of 10 clicks each, with 24 trains in each experimental condition. The EEG was sampled every 2 ms starting 20 ms before each click stimulus and continuing for a 500 ms epoch. These epochs were stored in digital form on LINC tape for later analysis. The computer program included tests for movement artefact overflows in the background EEG and in the AER. In the attending conditions the subject was instructed to respond to each click by closing a microswitch as fast as possible. The auditory RT was then displayed on a digital timer (Venner TSA 6614) during the ISI to give feed-back information, m the non-attending conditions, clicks were presented but were irrelevant to the subject's task; the digital timer was started by the computer and he was instructed to stop it as fast as he could. The visual RT could then be immediately read from the counter. In both conditions the subject was informed that he would be paid according to his performance. All the RTs were stored on LINC tape for later analysis. In the long ISI conditions the average inter-click ISI was 10 s, varying randomly from 8 to 12 s with a rectangular distribution. In the short ISI condition, the average ISI was
3 s, range 2.4 - 3.6 s. The visual ISI's had the same mean ISI as the clicks, but ranges were greater: 1 - 5 s in the short ISI condition, 4 - 16 s in the long ISI condition. These ranges prevented alternating presentation of the two types of stimuli. The computer was programmed not to start the counter within 0.5 s before or 1 s after the click. Regardless of the ISI, the ITI's had a mean of 30 s, varying randomly from 24 to 36 s. Each train was heralded by a red lamp, 1 m in front of the subject, which was switched on before the first stimulus, the interval corresponding to the ISI condition under study; it remained on until the end of the train. In the attending conditions the first stimulus was, of course, always a click, but in the other conditions either the click or the visual RT task could occur first. Averages were computed in two different ways. To study long-term or train-by-train changes of the responses over the whole experimental session, successive averages over 20 stimulus presentations (i.e., pairs of trains of stimuli) were calculated. The stimulus-by-stimulus or shortterm (within-train) changes were assessed by computing averages of all the first stimuli in the 24 trains, all the second stimuli, and so on. Thus, there were 12 train-bytrain and 10 stimulus-by-stimulus averages for each condition and subject. Amplitude and latencies were measured manually by setting cursors against the peaks of the averaged evoked response, as displayed on the LINC oscilloscope. Variances were also calculated and displayed as a check for artefacts. Four components were measured: (a) a positive peak with a latency range of 45 - 65 ms (PI); (b) a negative peak with a latency range of 80 -- 110 ms (N1); (c) a positive peak with a latency range of 160 - 220 ms (P2); and (d) a negative component with a latency range of 230 - 280 ms (N2). Latencies were taken for each of these four components, and amplitudes were taken as the difference between the negative and the positive peaks, i.e., PI -N1, Nt -P:, and P2-N2The reaction times were read off by the computer from the LINC tape and a 1000/x transformation carried out to give a speed measure. Average RTs train-by-train and stimulus-by-stimulus were computed as for the A E R data. The log conductance transformation was used for the skin resistance measure, and averages were computed train-bytrain and stimulus-by-stimulus as for the other measures. Trend analyses were used for statistical treatment of the data [6], trial number being thus a third factor after attention and ISI.
RESULTS
Average Eve ked Response Amplitude. The results with regard to amplitude are shown in Fig. 1,2, and 3, and in Table 1. There were highly significant changes with stimulus repetition both stimulusby-stimulus and train-by-train for P1-N1 and NI-P2. Both the linear and quadratic trends were significant, indicating a slightly curved decreasing function that did not reach an asymptote for the periods studied. For P2-N2 the decrease over time was significant only for the train-by-tram averages, showing a linear decrease over the whole experimental session. The effect of attention directed towards the stimuli as opposed to attention away from stimuli was very clear for the PI-NI and the N1-P2 amplitudes, with the former condition producing much bigger responses both
ATTENTION AND "HABITUATION" OF EVOKED RESPONSES
81
TABLE 1 F.mtios for AER amplitude Stimulus-by-stimulus averages Source
df
Pt-Nl
Nt-P2
Train-by-trainaverages P2-N2
Source
df
Repetition (R) Linear fiend
9/63 1/63
6.32?? 26.1277
5.6177 30.56??
1.06 0.35
Quadratic trend Attention (A) lnterstimulus interval (I) RX A Linear trend Quadratic trend RXI Linear trend Quadratic trend AXI RXAXI Linear trend Quadratic trend
1/63 1/7 1/7
24.75?? 26.72? 12.02"
16.7577 11.65" 7.84*
0.18 0.13 2.54
Repetition (R) 11/77 Linear trend 1/77 Quadratic trend 1/77 Attention (A) I/7 Interstimulus 1/7
9/63 1/63 1/63 9/63 1/63 1/63 1/7 9/63 1/63 1/63
5.03?? 29.18?? 0.18 1.59 7.401" 0.56 2.63 1.10 3.77 2.44
3.08? 15.3677 0.14 1.70 0.32 2.41 0.83 0.82 4.45* 0.05
0.84 0.01 0.01 0.99 1.81 0.02 0.32 0.71 0.00 1.34
interval (I) R XA I 1/77 Linear trend 1/77 Quadratic trend 1/77 RX1 11/77 Linear trend 1/77 Quadratic trend 1/77 AXI 1/7 RXAXI 11/77 Linear trend 1/77 Quadratic trend 1/77
P I-N 1
NI-P2
P2-N2
9.28tt 84.697t 11.187 35.1677 13.52?
18.17tt 159.1477 29.147 17.287 5.84*
S.36tt 50.44?? 0.08 0.04 1.94
1.49
1.97"
1.49
5.02* 0.43 2.25* 14.3577 0.80 3.27 1.20 0.29 0.07
18.15?? 0.12 3.617 31.3677 4.58* 2.39 1.32 6.93 0.50
13.2277 0.08 0.90 2.68 2.07 0.26 0.82 2.96 2.71
* p < 0.05 ? p <0.01 ? t p
25
20
~ 2o
E
o
~
I$
~
Io.
LU
i t Jr 30
Shmulus
Number
~l,lv • Attending 3sec. ~.s.i. • Non- attend ing 3 sec isi.
~
~
~
~
Shmulus
~
~
i
; ~o
Number • Attending 3see. e~,~ • N o n - attending 3 me, is? o Attending llOee¢ t,=,.
o Attending IOsec. ts.i = Non- attending 10sec.is i
e~hn~ lOeec~uti.
~ 2O
C 20
n° is
15 o
O. Pairs of Trains
FIG. 1. Effects of intexstimulus interval and direction of attention on the Pt-N 1 component of the auditory evoked response. Upper diagram: averaged stimulus-by-stimulus. Lower diagram: averaged pak-by-pair of trains.
Pairs of Trains
FIG. 2. Effects of interstimulus interval and direction of attention on the NI-P2 component of the auditory evoked response. Upper diagram: averaged stimulus-by-stimulus. Lower diauam: averaged pair-by-pair of trains.
82
C)HMAN AND LADER Uv 30
20
E &o ~s
~,° oJ S t imulus
Numbe:
#v 30 • A t t e n d i n g 3 s e c tsl
25
• Non-attending
3 sec is,
o A t t e n d m g l O s e c isl ~_ 20
a N o n - a t t e n d i n g IOsec msi
~J
Paws of
Trams
FIG. 3, Effects of interstimulus interval and direction of attention on the P2-N2 component of the auditory evoked response. Upper diagram: averaged stimulus-by-stimulus, Lower diagram: averaged pair-by-pair of trains. stimulus-by-stimulus and train-by-train. For the P2-N~, no effect was found in either of the two types of averages. Similarly, the ISI showed a statistically reliable effect for
Pt-NI and NI-P2, with higher response amplitudes for the long ISI, whereas P2-N 2 was not affected at all. Since some doubts have been raised concerning the utility of overall analyses in view of the marked individual differences in AER [ 1 7], individual analyses of variance with repetition as the error variance were carried out to test the between subject consistency of the effects of the attention and ISI variables in the train-by-train averages. The attention variable showed a highly consistent effect (Table 2): for both P]-NI and NI-P2 all subjects showed significant differences between the two attention conditions. The ISI variable was effective in producing amplitude differences in 6 of the subjects for the Pl -N1 amplitude, and in 5 for the N1-P2 amplitude. There were no attention × ISI interaction effects for any of the three amplitudes in the over-all analyses, and only two subjects showed such interactions in the individual analyses. For both PI-Nt and Nt-P2 there were significant repetition X attention interactions in the stimulus-bystimulus amplitude averages, attributable to a steeper linear slope in the attending conditions than in the non-attending conditions. The results for the train-by-train averages in this respect were similar to but not as clear-cut as those for within-train. For the repetition X ISI interaction both P]-NI and NI-P2 amplitudes showed significant linear components in the train-by-train analyses, which was due to a slightly more steep decrease in the 10 than in the 3 sec ISI. In the stimulus-by-stimulus analyses this hold true only for PI-N1. The only significant interection for P2-N2 was the linear repetition X attention interaction, primarily due to a more rapid decrease for the attending conditions. Latencies, Of the four peaks examined, the only latency to alter with stimulus repetition was stimulus-by-stimulus N1 (see Table 3), which occurred earlier with successive stimulus presentations. The peak occurred somewhat earlier if the subject attended to the stimuli. The P1 and P2 components also tended to have somewhat shorter latencies in the attending conditions, although the difference was significant at only the 0.1 level. In general, the results for the train-by-train averages were similar, but did not reach the 0.05 level of significance.
TABLE 2 Individual F-ratios for AER amplitude Subjects V.W. PI-NI Attention (A) Interstimulus interval (I) AXI
71.15tt 1.99 0.48
NI-P 2 A 1 A×I
8.o8~f 0.48 0.23
* p < 0.05 t P <0,01 t t p <0.001
P.J.N.
C.A.
G .B.
A.O.
G.N.
A.W.
J.J.K.
5 0 . 3 4 ~ - [ 12.70tt 141.60tt 36.77tt 23.34t! 3.15
33.75t~ 53.86+t 0.05
7.75+ 5.60* 0.31
3o.06tt 28.51tt 2.33
22.62t+ 0.25 0.01
38.94tt 64,lOft 2.72
70.17tJ151.88tt 14.48~t
5.97* 88.63J!0.02
4.53* 0.20 1.50
16.34tt 15.83t~ 19.59tt
5.02* 0.07 0.03
15,97++ 40;93tt 0.O1
4.53* 5.88* 2.04
ATTENTION AND "HABITUATION" OF EVOKED RESPONSES
83
TABLE 3 F-ratios for AER Latency Stimulus-by-stimulus average
df
PI
9/63 1/7 1/7 9/63 9/63 1/7 9/63
Source Repetition (R) Attention (A) Interstimulus interval (I) RXA RXI AXI RXAXI
Train-by-train average
NI
P2
N2
df
PI
NI
P2
N2
1.36 3.63 0.31
3.021" 6.89* 3.58
0.57 3.96 1.70
0.76 0.19 0.31
11/77 1/7 117
1.02 3.10 1.04
0.74 5.16 4.10
0.88 0.49 0.20
0.98 0.64 1.37
0.35 0.90 0.78 0.90
0.97 1.38 0.31 0.76
1.85 0.47 1.04 1.19
0.51 0.89 4.69 0.35
11/77 11/77 1/7 11/77
0.93 0.96 0.31 0.71
0.50 0.84 0.28 1.06
1.31 1.50 2.93 0.78
0.59 1.05 5.82* 2.41
* p <0.05 t t, <0.01
Reaction-time Reaction-times were more rapid to the later stimuli within trains (F9,63 = 2.58; p < 0.05), especially for the short ISI (as shown by a significant repetition X ISI interaction: F9,63 = 2.28; p < 0.05). Overall, reactions were faster for the short than for the long ISI ( F I , 7 - 1 8 . 6 3 ; p < 0.01). The attention effect, of course, is irrelevant since it only reflects the difference in RT to stimuli of different modality. The train-by-train analysis showed no effect of repetition indicating a very stable performance level over the whole experimental session. The only significant effect in the train-by-train analysis was that of the ISI, ( F I . 7 = 18.28; p < 0.01), indicating faster reactions with the short ISI. Skin Conductance Level The within train trend in SCL showed a significant drop over the course of the 10 stimuli (F9,63 = 4 . 1 3 ; p <(0.01). A significant repetition X ISI interaction (F9,63 - 6.34; p <( 0.01) indicates that this trend was more pronounced for the long than for the short ISI. Neither the factors of attention or the ISI produced any within train effects. The train-bytrain analysis showed no significant effect at all, the SCL being fairly stable throughout the experimental session.
DISCUSSION The results o f the present study showed that the PI-NI and N1-P2 potentials of the AER were greater when subjects attended to stimuli than when their attention was directed away from stimuli. Long ISI was also associated with bigger responses than was a relatively short ISI. Furthermore, a strong over-all decremental effect was found both in the analyses stimulus-by-stimulus and trainby-train. Thus, the AER decreased with stimulus repetition even when the ISI was long and the subject paid attention to the stimulus.
The significant repetition X attention interaction was due not to a more rapid decrease in the non-attending condition as might have been expected, but to a steeper decline in the attending conditions, although the difference was not very pronounced (see Figs. 1 and 2). This held for b o t h the stimulus-by-stimulus and the train-by-train analyses. Again contrary to expectation, the repetition X ISI interaction was due to a more pronounced decrease with the long than with the short ISI, both in the stimulus-bystimulus and train-by-train analyses. Both these results, however, can be attributed to converging rather than diverging trends, i.e., both the attended and the long ISI conditions started at a higher amplitude level and then dropped toward the levels of the non-attended and short ISI conditions. Thus, something like a "Law of Initial Values" seems to operate in AER response decrement with bigger initial responses being associated with more rapid decrease as the stimuli progress. The interpretation of amplitude decrements of the AER is difficult, since this response cannot be genuinely studied from trial to trial except in subjects with exceptionally clear evoked responses. To infer such changes, indirect methods must be used which invariably introduce restricting assumptions. In averaging across trains to study stimulus-by-stimulus (within-train) changes, these assumptions may not be met if there are lasting decrementai effects from one train to the next, since the procedure implies that exactly the same process is operating in each train. The significant train-by-train decrement thus calls for careful and tentative interpretations o f our results. Therefore, the steeper slope within trains for the long ISI and the attending conditions cannot be simply interpreted to imply more rapid amplitude attenuations during these conditions, since the response in the short ISI and non-attending conditions might have reached a relatively stable amplitude level in the first few presentations. The safest conclusion, then, is that response decrement of the AER takes place even if the subject attends to the stimuli or the ISI is long. Thus, the effect of attention on the A E R [e.g. 2, 5, 8, 9, 10, 11, 17, 22, 24] seems n o t t o be attributable to a more
84
OHMAN AND LADER
rapid amplitude decrement in the non-attending conditions. With regard to the ISI the present results are not in accord with previous ones: in general with an ISI of about 3 s a rapid exponential response decrease occurs which reaches an asymptote of less than half the initial amplitude after about 3 or 4 stimuli [7, 20]. In our study, subjects when attending to the stimuli showed a slightly curved decreasing function which continued downwards over all 10 stimuli, and subjects when not attending to the stimuli showed little decrease. These discrepancies in results can probably be attributed to one or more differences in experimental conditions but it seems that the exponential decrease previously described is not general or perhaps even typical. The inclusion of measures of RT and SCL in the experimental design permits some general comparisons between various indices of activation [cf. 25]. There was no clearcut counterpart in the other two measures to the general decreasing trends of the AER. For the stimulus-bystimulus averages there was a tendency toward a lowering of the SCL, whereas the RT showed an opposite change, i.e. response speed increased with stimuli, which probably could be attributed to a within-train warming-up effect. The common repetition X ISI interaction, however, suggested some similarity in effects of ISI on change over stimuli in the SCL and RT measures. Presumably due to the immediate feed-back of performance [4, 16], both the SCL and the RT remained at a relatively stable level throughout the experimental session as i n d i c a t e d b y the train-by-train analyses. Thus, the decrement of the AER over successive stimuli is not in general explicable solely in terms of a decrease in general, diffuse activation. The fact that the AER seem to be sensitive to changes in activation makes a control of this variable important in any study of the effect of attention. The P1-N~-P 2 complex shows a direct relationship with activation [5, 10l, and the P2-N2 an inverse one [27]. The latter component, furthermore, seem to be a very sensitive indicator of moment-tomoment shifts in activation [1]. Since the attention variable affected neither the P2-N2 nor the SCL in the present experiment, the effect on PI-NI and Nt-P2 should be attributable to differences in the attention paid to the clicks when they were relevant and irrelevant for the subject's task. Recently, the need for an attention concept to account for results such as ours has been questioned by N~/it/inen [17, 18] and by Karlin [13]. Basically, two arguments have been used. Firstly, since most of the studies demonstratinz an attention effect have used regular stimulus presentations [e.g. 2, 22, 24] it is argued that the effect on the AER is
due to an accurately timed preparatory, unspecific arousal to the relevant stimuli. In support of this notion N/i~it/inen [17] demonstrated that the effect of selective attention disappeared if the relevant stimuli could not be accurately predicted. Secondly, Karlin [13] introduced the reactive change hypothesis, which postulates a decrease in arousal level following a relevant stimulus because it is judged as unlikely to be immediately followed by another relevant stimulus, or because of a "task completion relaxation". This change in activation level is believed to give rise to a p o s i t i v e component of long but varying latency (300-550 ms). However, none of these arguments seem to be applicable to the data of the present experiment. While it was just possible for the subjects to predict the relevant stimulus in the short ISI condition, this was virtually impossible with the long tSI. Yet the effect of attention was significant for every subject for the PI-N~ and N1-P2 amplitudes (see table 2). Neither does the reactive change hypothesis apply, because the attention effect was apparent even in the early P1-N1 component. Karlin admits that his hypothesis "probably could not explain enhancement of components with latencies shorter than the magnitude expected from RT studies" [ 13 ], p. 13 2. A further possible explanation for our results without invoking a concept of attention pertains to the effect of the motor response to the clicks in the attending but not in the non-attending conditions. Recently, Karlin et aL [14] demonstrated a general negative displacement of the AER to stimuli to which a response was required. This effect was significant for the NI, P2 and N 2 components, but not for the Pt. Consequently, this effect might have contributed to the strong effect which we found of attention of the P~-N~ amplitude, but not to the effect on N1-P2, since the latter components seem to have been displaced to about an equal extent in Karlin et al.'s data. As none of the alternative explanations seem to account for our data, the effect of attention which we observed are best explained in terms of selective tuning of an attended sensory modality. There is one final point of interest. In the figures for the stimulus-by-stimulus averages it can be seen that the difference between the long and short ISis is present even to the first stimulus in the train, especially in the non-attending condition. And yet the interval before the first stimulus was always between 24 and 36 s.The warning light could not give an accurate indication of the onset of the first click because the interval was random and in the non-attending conditions the first stimulus could equally well be the visual task and not the click. The intriguing possibility that set can modify brain responses under such experimental parameters is at present under investigation.
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enceph, clin. Neurophysiol. 28: 153-161, 1970.
ATI'ENTION AND "HABITUATION" OF EVOKED RESPONSES 8. Garcia-Ausst, E., J. Bogacz and A. Vanzulli. Significance of the photic stimulus on the evoked response in man. In: Brain Mechanisms and Learning, edited by J . F . Delafresnaye. Oxford, BlackweU, 1961, pp. 603-623. 9. Garcia-Ausst, E., J. Bogacz and A. Vanzulli. Effects of attention and inattention upon visual evoked response. Electroenceph, clin. Neurophysiol. 17: 136-143, 1964. 10. Groves, P.M. and R.G. Eason. Effects of attention and activation on the visual evoked cortical potential and reaction time. Psychophysiology 5: 394-398, 1969. 11. Haider, M., P. Spong and D. B. Lindsley. Attention, vigilance, and cortical evoked 1-1 potentials in humans. Science 145: 180-182, 1964. 12. Hernandez-Peon, R. Neurophysiological correlates of habituation and other manifestations of plastic inhibition (internal inhibition). Electroenceph. clin. Neurophysiol. Suppl. 13: 101-114, 1960. 13. Karlin, L. Cognition, preparation, and sensory evoked potentials. Psychol. Bull. 73: 122-136, 1970. 14. Karlin, L., M.J. Martz and A.M. Mordkoff. Motor performance and sensory 1-1 evoked potentials. Electroenceph. clin, Neurophysioi. 28: 307-313, 1970. 15. Lader, M.H. and L. Wing. Physiological Measures, Sedative Drugs and Morbid Anxiety. London: Oxford University Press, 1966. 16. Mackworth, J.F. Vigilance and Habituation. Hamondsworth: Penguin, 1969. 17. Nfi'~t~nen, R. Selective attention and evoked potentials. Ann. Acad. Sci. fenn. B151, 1:226 pp, 1967. 18. N~t~'nen, R. Anticipation of relevant stimuli and evoked potentials: A comment on Donchin's and Cohen's "Average evoked potentials and intramodal selective attention". Percept. Mot. Skills 28: 639-646, 1969.
85 19. Perry, N.W. and R.M. Copenhaver. Differential conical habituation with stimulation of central and peripheral retina. Percept. Mot. Skills 20: 1209-1213, 1965. 20. Ritter, W., H.G. Vaughan and L.D. Costa. Orienting and habituation to auditory stimufi: A study of short term changes in average evoked responses. Electroenceph. clin. NeurophysioL 25: 550-556, 1968. 21. Roth, W. T. and B. S. Kopoll. The auditory evoked response to repeated stimuli during a vigilance task. Psychophysiology 6: 301-309, 1969. 22. Satterfield, J.H. Evoked cortical response enhancement and attention in man. A study of responses to auditory and shock stimufi. Electroenceph. clin. Neurophysiol. 19: 470-475, 1965. 23. Sokolov, E.N. Perception and the Conditioned Reflex. London: Pergamon Press, 1963. 24. Spong, P., M. Halder and D. B. Lindsley. Selective attentiveness and cortical evoked responses to visual and auditory stimuli. Science 148: 395-397, 1965.5. 25. Sutton, S. The specification of psychological variables in an average evoked potential experiment. In: Average Evoked Potentials. Methods, Results, and Evaluations, edited by E. Donchin and D. B. Lindsley. Washington, D.C.: Office of Technology Utilization, NASA, 1969. 26. Walter, W.G. The convergence and interaction of visual, auditory and tactile responses in human non-specific cortex. In: Sensory Evoked Responses in Man. Ann. N.Y. Acad. Sci. 112: 320-361, 1964. 27. Wilkinson, R. T. and H. C. Morlock. Auditory evoked response and reaction time. Electroenceph. clin. Neurophysiol. 23: 50-56, 1967.
Selective Attention and "Habituation" of the Auditory Averaged Evoked Response in Humans'" ARNE ()HMAN 3 AND MALCOLM L A D E R 4
Institute o f Psychiatry, University o f London, Denmark Hill, London S.E. 5, U..K.
(Received 6 July 1971) OHMAN, A. AND M. H. LADER. Selective attention and "habituation" of the auditory averaged evoked responl¢ in humans. PHYSIOL. BEHAV. 8 (1) 79-85, 1972.-The study examined the effects of dixeettoa of attention and interstimulus interval on the rate of amplitude decrement over time of the vertex auditory evoked response in hummu. Short-term or stimulus-by-stimulus changes were studied by averaging aczoss 24 disczetely pteNnted ttsim each of 10 click stimuli. Long-term or train-by-train changes were studied by averaging over successive pairs of traim. Wlum atteadhl$ to the clicks, the subject performed a reaction-time (RT) task with the crick as stimulus; when i p m ' i ~ the dic3~ he peffmmed RTs to a visual stimulus. Both RT tasks were performed with irregular inte~ttlmulu$ intervals of 2.4 - 3.6 and 8 - 12 s, each of the 8 subjects being thus studied on four occasions. Atteading to the stimuli and long iatent~ult~t iatervals enhanced the PI-Nt-P2 components. Amplitude decreased over time both for Jtimulus-by-~]mulu lead tmia-by.ttatn averages. Somewhat unexpectedly, there was a slight but significant tendency towards a steeper slope for the attending and long interstimulus interval conditions, probably following on the larger initial responses for these condiiiem. Auditory average evoked response
Response decrement over time
Habituation
Attention
lnter~timuhis interval
On a more theoretical level, the response decrement of the AER could have clear psychological correlates, tending to suggest a psychological mechan~m, o r it couJd be due to a more fundamental physiological mechanism such as neuronal recovery processes [20, 21 ; see also 3] . A putative psychological correlate is change in attention, or more specifically, distraction. Sokolov [ 2 3 ] , for example, suggested that the ork.lting responses to s t i m u l i t o which the subject attended habituated much more slowly than the responses to non-attended stimuli. Furthermore, Hernandez-Peon [l 2] and Walter [26] have implied that a similar relationship holds for the evoked potentials, i.e. one would expect the time course of response attenuation with repeated stimuli to differ according to whether attention directed toward or away from the stimuli. Thus, the effect of attention on AER amplitude [e.g. 2, 5, 8, 9, 10, I I , 17, 22, 24] could result from less respoose decrement in the attending than in the non-attending conditions, rather than from a direct effect of attention on response amplitucle. In the present study an a t t e m p t ]ms been made to delineate some o f the parameters controlling both shortand long-term changes in AER amplitude. Our main concern was with direction of attention, but since previous studies have indicated that interstimulus interval is another critical factor governing response attenuation [7, 20, 21],
IN SEVERAL recent studies of the averaged evoked response (AER) in humans, a drop in size o f the later potentials has been apparent as the stimuli were repeated, usually in the form of a slow, long-term change over several hundred stimulus presentations [8, 9, l l, 19]. Ritter et al. [20] introduced a method to study short-term or stimulus-by-stimulus changes by averaging across discretely presented trains o f stimuli, with an intertrain interval (ITI) of sufficient length to ensure complete recovery of the response between trains [cf. 3 ]. When a short interstimulus interval (ISI) was used, a very rapid decrement Over the.first few stimuli within a train was observed [7, 20, 21 ]. The inconstancy of the AER over stimulus presentations, with its systematic decreasing trend in amplitude, has important implications. F o r the averaging procedure to be justified, it must be assumed that the electroencephalographic activity that is time-locked to the stimulus remains fairly constant while the background EEG randomizes out. As the data seem to indicate that the time-locked activity does change with stimulus repetition, it is very important to elucidate the parameters which control these changes. Furthermore, any effect o f a variable on AER amplitude could be due either to a direct effect on response size or to an indirect effect on the rate of response decrement, since the AER by definition is derived from many trials.
2 Supported by the Medical Research Council of Great Britain. Requests for reprints should be addressed to M. Lader. 3Supported by a scholarship from the British Council and by travel grants from the Wallenb~g foundation. Present address: Department of Psychology, University of Uppsala, Svarth~'cksgatan I0, ,$-753 30 Uppmla, Sweden. 4Member of External Scientific Staff, Medical Research Council. 79
80
OHMAN AND LADER
this variable was also manipulated. In order to control for changes in general activation and performance, skin conductance level (SCL) and reaction-time (RT) were included as dependent variables. METHOD A total of 10 paid volunteer subjects, 3 females and 7 males (age range 22-33 years), including the authors, participated in the experiment. Two subjects were replaced after taking part in the first experimental condition because of small indistinct evoked responses, thus leaving complete data for 8 subjects. The subjects were members of the laboratory staff, and all but two had previously acted as subjects in experiments involving AER and reaction time. The subject was comfortably seated w i t h his eyes open and in a sound-protected room; the recording equipment was in an adjacent room. The experimental procedure was outlined and he was particularly instructed to avoid movements during the trains of stimuli. The experiment was performed on-line using a LINC-8 computer, which presented the stimuli, calculated and displayed reaction times (RTs), computed random ITIs and ISis, and sampled the EEG and skin resistance. The EEG was recorded from bipolar saline pad electrodes (Cz - T 3 on the 10-20 system) and fed through a Grass 511C amplifier of band-pass 0.3-1000 Hz to the A-D converter input of the LINC-8 computer. Skin conductance level (SCL) was recorded as resistance using double-element electrodes | 1 5 ] , the computer sampling the skin resistance immediately before each stimulus. The basic design was a 2 X 2 factorial, with attending vs. non-attending to auditory stimuli as one factor, and two different ISI's as the other. Thus, each subject was studied on four different occasions. The order of presentation of conditions was counterbalanced so that each condition preceded or followed all other conditions an equal n u m b e r of times. The between condition interval for a subject was at least 3 days. In all the conditions, auditory evoked responses were measured to clicks of about 70 db intensity and 1 ms in duration presented through a loudspeaker behind the subject. The stimuli appeared in trains of 10 clicks each, with 24 trains in each experimental condition. The EEG was sampled every 2 ms starting 20 ms before each click stimulus and continuing for a 500 ms epoch. These epochs were stored in digital form on LINC tape for later analysis. The computer program included tests for movement artefact overflows in the background EEG and in the AER. In the attending conditions the subject was instructed to respond to each click by closing a microswitch as fast as possible. The auditory RT was then displayed on a digital timer (Venner TSA 6614) during the ISI to give feed-back information, m the non-attending conditions, clicks were presented but were irrelevant to the subject's task; the digital timer was started by the computer and he was instructed to stop it as fast as he could. The visual RT could then be immediately read from the counter. In both conditions the subject was informed that he would be paid according to his performance. All the RTs were stored on LINC tape for later analysis. In the long ISI conditions the average inter-click ISI was 10 s, varying randomly from 8 to 12 s with a rectangular distribution. In the short ISI condition, the average ISI was
3 s, range 2.4 - 3.6 s. The visual ISI's had the same mean ISI as the clicks, but ranges were greater: 1 - 5 s in the short ISI condition, 4 - 16 s in the long ISI condition. These ranges prevented alternating presentation of the two types of stimuli. The computer was programmed not to start the counter within 0.5 s before or 1 s after the click. Regardless of the ISI, the ITI's had a mean of 30 s, varying randomly from 24 to 36 s. Each train was heralded by a red lamp, 1 m in front of the subject, which was switched on before the first stimulus, the interval corresponding to the ISI condition under study; it remained on until the end of the train. In the attending conditions the first stimulus was, of course, always a click, but in the other conditions either the click or the visual RT task could occur first. Averages were computed in two different ways. To study long-term or train-by-train changes of the responses over the whole experimental session, successive averages over 20 stimulus presentations (i.e., pairs of trains of stimuli) were calculated. The stimulus-by-stimulus or shortterm (within-train) changes were assessed by computing averages of all the first stimuli in the 24 trains, all the second stimuli, and so on. Thus, there were 12 train-bytrain and 10 stimulus-by-stimulus averages for each condition and subject. Amplitude and latencies were measured manually by setting cursors against the peaks of the averaged evoked response, as displayed on the LINC oscilloscope. Variances were also calculated and displayed as a check for artefacts. Four components were measured: (a) a positive peak with a latency range of 45 - 65 ms (PI); (b) a negative peak with a latency range of 80 -- 110 ms (N1); (c) a positive peak with a latency range of 160 - 220 ms (P2); and (d) a negative component with a latency range of 230 - 280 ms (N2). Latencies were taken for each of these four components, and amplitudes were taken as the difference between the negative and the positive peaks, i.e., PI -N1, Nt -P:, and P2-N2The reaction times were read off by the computer from the LINC tape and a 1000/x transformation carried out to give a speed measure. Average RTs train-by-train and stimulus-by-stimulus were computed as for the A E R data. The log conductance transformation was used for the skin resistance measure, and averages were computed train-bytrain and stimulus-by-stimulus as for the other measures. Trend analyses were used for statistical treatment of the data [6], trial number being thus a third factor after attention and ISI.
RESULTS
Average Eve ked Response Amplitude. The results with regard to amplitude are shown in Fig. 1,2, and 3, and in Table 1. There were highly significant changes with stimulus repetition both stimulusby-stimulus and train-by-train for P1-N1 and NI-P2. Both the linear and quadratic trends were significant, indicating a slightly curved decreasing function that did not reach an asymptote for the periods studied. For P2-N2 the decrease over time was significant only for the train-by-tram averages, showing a linear decrease over the whole experimental session. The effect of attention directed towards the stimuli as opposed to attention away from stimuli was very clear for the PI-NI and the N1-P2 amplitudes, with the former condition producing much bigger responses both
ATTENTION AND "HABITUATION" OF EVOKED RESPONSES
81
TABLE 1 F.mtios for AER amplitude Stimulus-by-stimulus averages Source
df
Pt-Nl
Nt-P2
Train-by-trainaverages P2-N2
Source
df
Repetition (R) Linear fiend
9/63 1/63
6.32?? 26.1277
5.6177 30.56??
1.06 0.35
Quadratic trend Attention (A) lnterstimulus interval (I) RX A Linear trend Quadratic trend RXI Linear trend Quadratic trend AXI RXAXI Linear trend Quadratic trend
1/63 1/7 1/7
24.75?? 26.72? 12.02"
16.7577 11.65" 7.84*
0.18 0.13 2.54
Repetition (R) 11/77 Linear trend 1/77 Quadratic trend 1/77 Attention (A) I/7 Interstimulus 1/7
9/63 1/63 1/63 9/63 1/63 1/63 1/7 9/63 1/63 1/63
5.03?? 29.18?? 0.18 1.59 7.401" 0.56 2.63 1.10 3.77 2.44
3.08? 15.3677 0.14 1.70 0.32 2.41 0.83 0.82 4.45* 0.05
0.84 0.01 0.01 0.99 1.81 0.02 0.32 0.71 0.00 1.34
interval (I) R XA I 1/77 Linear trend 1/77 Quadratic trend 1/77 RX1 11/77 Linear trend 1/77 Quadratic trend 1/77 AXI 1/7 RXAXI 11/77 Linear trend 1/77 Quadratic trend 1/77
P I-N 1
NI-P2
P2-N2
9.28tt 84.697t 11.187 35.1677 13.52?
18.17tt 159.1477 29.147 17.287 5.84*
S.36tt 50.44?? 0.08 0.04 1.94
1.49
1.97"
1.49
5.02* 0.43 2.25* 14.3577 0.80 3.27 1.20 0.29 0.07
18.15?? 0.12 3.617 31.3677 4.58* 2.39 1.32 6.93 0.50
13.2277 0.08 0.90 2.68 2.07 0.26 0.82 2.96 2.71
* p < 0.05 ? p <0.01 ? t p
25
20
~ 2o
E
o
~
I$
~
Io.
LU
i t Jr 30
Shmulus
Number
~l,lv • Attending 3sec. ~.s.i. • Non- attend ing 3 sec isi.
~
~
~
~
Shmulus
~
~
i
; ~o
Number • Attending 3see. e~,~ • N o n - attending 3 me, is? o Attending llOee¢ t,=,.
o Attending IOsec. ts.i = Non- attending 10sec.is i
e~hn~ lOeec~uti.
~ 2O
C 20
n° is
15 o
O. Pairs of Trains
FIG. 1. Effects of intexstimulus interval and direction of attention on the Pt-N 1 component of the auditory evoked response. Upper diagram: averaged stimulus-by-stimulus. Lower diagram: averaged pak-by-pair of trains.
Pairs of Trains
FIG. 2. Effects of interstimulus interval and direction of attention on the NI-P2 component of the auditory evoked response. Upper diagram: averaged stimulus-by-stimulus. Lower diauam: averaged pair-by-pair of trains.
82
C)HMAN AND LADER Uv 30
20
E &o ~s
~,° oJ S t imulus
Numbe:
#v 30 • A t t e n d i n g 3 s e c tsl
25
• Non-attending
3 sec is,
o A t t e n d m g l O s e c isl ~_ 20
a N o n - a t t e n d i n g IOsec msi
~J
Paws of
Trams
FIG. 3, Effects of interstimulus interval and direction of attention on the P2-N2 component of the auditory evoked response. Upper diagram: averaged stimulus-by-stimulus, Lower diagram: averaged pair-by-pair of trains. stimulus-by-stimulus and train-by-train. For the P2-N~, no effect was found in either of the two types of averages. Similarly, the ISI showed a statistically reliable effect for
Pt-NI and NI-P2, with higher response amplitudes for the long ISI, whereas P2-N 2 was not affected at all. Since some doubts have been raised concerning the utility of overall analyses in view of the marked individual differences in AER [ 1 7], individual analyses of variance with repetition as the error variance were carried out to test the between subject consistency of the effects of the attention and ISI variables in the train-by-train averages. The attention variable showed a highly consistent effect (Table 2): for both P]-NI and NI-P2 all subjects showed significant differences between the two attention conditions. The ISI variable was effective in producing amplitude differences in 6 of the subjects for the Pl -N1 amplitude, and in 5 for the N1-P2 amplitude. There were no attention × ISI interaction effects for any of the three amplitudes in the over-all analyses, and only two subjects showed such interactions in the individual analyses. For both PI-Nt and Nt-P2 there were significant repetition X attention interactions in the stimulus-bystimulus amplitude averages, attributable to a steeper linear slope in the attending conditions than in the non-attending conditions. The results for the train-by-train averages in this respect were similar to but not as clear-cut as those for within-train. For the repetition X ISI interaction both P]-NI and NI-P2 amplitudes showed significant linear components in the train-by-train analyses, which was due to a slightly more steep decrease in the 10 than in the 3 sec ISI. In the stimulus-by-stimulus analyses this hold true only for PI-N1. The only significant interection for P2-N2 was the linear repetition X attention interaction, primarily due to a more rapid decrease for the attending conditions. Latencies, Of the four peaks examined, the only latency to alter with stimulus repetition was stimulus-by-stimulus N1 (see Table 3), which occurred earlier with successive stimulus presentations. The peak occurred somewhat earlier if the subject attended to the stimuli. The P1 and P2 components also tended to have somewhat shorter latencies in the attending conditions, although the difference was significant at only the 0.1 level. In general, the results for the train-by-train averages were similar, but did not reach the 0.05 level of significance.
TABLE 2 Individual F-ratios for AER amplitude Subjects V.W. PI-NI Attention (A) Interstimulus interval (I) AXI
71.15tt 1.99 0.48
NI-P 2 A 1 A×I
8.o8~f 0.48 0.23
* p < 0.05 t P <0,01 t t p <0.001
P.J.N.
C.A.
G .B.
A.O.
G.N.
A.W.
J.J.K.
5 0 . 3 4 ~ - [ 12.70tt 141.60tt 36.77tt 23.34t! 3.15
33.75t~ 53.86+t 0.05
7.75+ 5.60* 0.31
3o.06tt 28.51tt 2.33
22.62t+ 0.25 0.01
38.94tt 64,lOft 2.72
70.17tJ151.88tt 14.48~t
5.97* 88.63J!0.02
4.53* 0.20 1.50
16.34tt 15.83t~ 19.59tt
5.02* 0.07 0.03
15,97++ 40;93tt 0.O1
4.53* 5.88* 2.04
ATTENTION AND "HABITUATION" OF EVOKED RESPONSES
83
TABLE 3 F-ratios for AER Latency Stimulus-by-stimulus average
df
PI
9/63 1/7 1/7 9/63 9/63 1/7 9/63
Source Repetition (R) Attention (A) Interstimulus interval (I) RXA RXI AXI RXAXI
Train-by-train average
NI
P2
N2
df
PI
NI
P2
N2
1.36 3.63 0.31
3.021" 6.89* 3.58
0.57 3.96 1.70
0.76 0.19 0.31
11/77 1/7 117
1.02 3.10 1.04
0.74 5.16 4.10
0.88 0.49 0.20
0.98 0.64 1.37
0.35 0.90 0.78 0.90
0.97 1.38 0.31 0.76
1.85 0.47 1.04 1.19
0.51 0.89 4.69 0.35
11/77 11/77 1/7 11/77
0.93 0.96 0.31 0.71
0.50 0.84 0.28 1.06
1.31 1.50 2.93 0.78
0.59 1.05 5.82* 2.41
* p <0.05 t t, <0.01
Reaction-time Reaction-times were more rapid to the later stimuli within trains (F9,63 = 2.58; p < 0.05), especially for the short ISI (as shown by a significant repetition X ISI interaction: F9,63 = 2.28; p < 0.05). Overall, reactions were faster for the short than for the long ISI ( F I , 7 - 1 8 . 6 3 ; p < 0.01). The attention effect, of course, is irrelevant since it only reflects the difference in RT to stimuli of different modality. The train-by-train analysis showed no effect of repetition indicating a very stable performance level over the whole experimental session. The only significant effect in the train-by-train analysis was that of the ISI, ( F I . 7 = 18.28; p < 0.01), indicating faster reactions with the short ISI. Skin Conductance Level The within train trend in SCL showed a significant drop over the course of the 10 stimuli (F9,63 = 4 . 1 3 ; p <(0.01). A significant repetition X ISI interaction (F9,63 - 6.34; p <( 0.01) indicates that this trend was more pronounced for the long than for the short ISI. Neither the factors of attention or the ISI produced any within train effects. The train-bytrain analysis showed no significant effect at all, the SCL being fairly stable throughout the experimental session.
DISCUSSION The results o f the present study showed that the PI-NI and N1-P2 potentials of the AER were greater when subjects attended to stimuli than when their attention was directed away from stimuli. Long ISI was also associated with bigger responses than was a relatively short ISI. Furthermore, a strong over-all decremental effect was found both in the analyses stimulus-by-stimulus and trainby-train. Thus, the AER decreased with stimulus repetition even when the ISI was long and the subject paid attention to the stimulus.
The significant repetition X attention interaction was due not to a more rapid decrease in the non-attending condition as might have been expected, but to a steeper decline in the attending conditions, although the difference was not very pronounced (see Figs. 1 and 2). This held for b o t h the stimulus-by-stimulus and the train-by-train analyses. Again contrary to expectation, the repetition X ISI interaction was due to a more pronounced decrease with the long than with the short ISI, both in the stimulus-bystimulus and train-by-train analyses. Both these results, however, can be attributed to converging rather than diverging trends, i.e., both the attended and the long ISI conditions started at a higher amplitude level and then dropped toward the levels of the non-attended and short ISI conditions. Thus, something like a "Law of Initial Values" seems to operate in AER response decrement with bigger initial responses being associated with more rapid decrease as the stimuli progress. The interpretation of amplitude decrements of the AER is difficult, since this response cannot be genuinely studied from trial to trial except in subjects with exceptionally clear evoked responses. To infer such changes, indirect methods must be used which invariably introduce restricting assumptions. In averaging across trains to study stimulus-by-stimulus (within-train) changes, these assumptions may not be met if there are lasting decrementai effects from one train to the next, since the procedure implies that exactly the same process is operating in each train. The significant train-by-train decrement thus calls for careful and tentative interpretations o f our results. Therefore, the steeper slope within trains for the long ISI and the attending conditions cannot be simply interpreted to imply more rapid amplitude attenuations during these conditions, since the response in the short ISI and non-attending conditions might have reached a relatively stable amplitude level in the first few presentations. The safest conclusion, then, is that response decrement of the AER takes place even if the subject attends to the stimuli or the ISI is long. Thus, the effect of attention on the A E R [e.g. 2, 5, 8, 9, 10, 11, 17, 22, 24] seems n o t t o be attributable to a more
84
OHMAN AND LADER
rapid amplitude decrement in the non-attending conditions. With regard to the ISI the present results are not in accord with previous ones: in general with an ISI of about 3 s a rapid exponential response decrease occurs which reaches an asymptote of less than half the initial amplitude after about 3 or 4 stimuli [7, 20]. In our study, subjects when attending to the stimuli showed a slightly curved decreasing function which continued downwards over all 10 stimuli, and subjects when not attending to the stimuli showed little decrease. These discrepancies in results can probably be attributed to one or more differences in experimental conditions but it seems that the exponential decrease previously described is not general or perhaps even typical. The inclusion of measures of RT and SCL in the experimental design permits some general comparisons between various indices of activation [cf. 25]. There was no clearcut counterpart in the other two measures to the general decreasing trends of the AER. For the stimulus-bystimulus averages there was a tendency toward a lowering of the SCL, whereas the RT showed an opposite change, i.e. response speed increased with stimuli, which probably could be attributed to a within-train warming-up effect. The common repetition X ISI interaction, however, suggested some similarity in effects of ISI on change over stimuli in the SCL and RT measures. Presumably due to the immediate feed-back of performance [4, 16], both the SCL and the RT remained at a relatively stable level throughout the experimental session as i n d i c a t e d b y the train-by-train analyses. Thus, the decrement of the AER over successive stimuli is not in general explicable solely in terms of a decrease in general, diffuse activation. The fact that the AER seem to be sensitive to changes in activation makes a control of this variable important in any study of the effect of attention. The P1-N~-P 2 complex shows a direct relationship with activation [5, 10l, and the P2-N2 an inverse one [27]. The latter component, furthermore, seem to be a very sensitive indicator of moment-tomoment shifts in activation [1]. Since the attention variable affected neither the P2-N2 nor the SCL in the present experiment, the effect on PI-NI and Nt-P2 should be attributable to differences in the attention paid to the clicks when they were relevant and irrelevant for the subject's task. Recently, the need for an attention concept to account for results such as ours has been questioned by N~/it/inen [17, 18] and by Karlin [13]. Basically, two arguments have been used. Firstly, since most of the studies demonstratinz an attention effect have used regular stimulus presentations [e.g. 2, 22, 24] it is argued that the effect on the AER is
due to an accurately timed preparatory, unspecific arousal to the relevant stimuli. In support of this notion N/i~it/inen [17] demonstrated that the effect of selective attention disappeared if the relevant stimuli could not be accurately predicted. Secondly, Karlin [13] introduced the reactive change hypothesis, which postulates a decrease in arousal level following a relevant stimulus because it is judged as unlikely to be immediately followed by another relevant stimulus, or because of a "task completion relaxation". This change in activation level is believed to give rise to a p o s i t i v e component of long but varying latency (300-550 ms). However, none of these arguments seem to be applicable to the data of the present experiment. While it was just possible for the subjects to predict the relevant stimulus in the short ISI condition, this was virtually impossible with the long tSI. Yet the effect of attention was significant for every subject for the PI-N~ and N1-P2 amplitudes (see table 2). Neither does the reactive change hypothesis apply, because the attention effect was apparent even in the early P1-N1 component. Karlin admits that his hypothesis "probably could not explain enhancement of components with latencies shorter than the magnitude expected from RT studies" [ 13 ], p. 13 2. A further possible explanation for our results without invoking a concept of attention pertains to the effect of the motor response to the clicks in the attending but not in the non-attending conditions. Recently, Karlin et aL [14] demonstrated a general negative displacement of the AER to stimuli to which a response was required. This effect was significant for the NI, P2 and N 2 components, but not for the Pt. Consequently, this effect might have contributed to the strong effect which we found of attention of the P~-N~ amplitude, but not to the effect on N1-P2, since the latter components seem to have been displaced to about an equal extent in Karlin et al.'s data. As none of the alternative explanations seem to account for our data, the effect of attention which we observed are best explained in terms of selective tuning of an attended sensory modality. There is one final point of interest. In the figures for the stimulus-by-stimulus averages it can be seen that the difference between the long and short ISis is present even to the first stimulus in the train, especially in the non-attending condition. And yet the interval before the first stimulus was always between 24 and 36 s.The warning light could not give an accurate indication of the onset of the first click because the interval was random and in the non-attending conditions the first stimulus could equally well be the visual task and not the click. The intriguing possibility that set can modify brain responses under such experimental parameters is at present under investigation.
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