- Email: [email protected]
Selective attention, contingent negative variation and the evoked potential
Biological
Psychology,
SELECTlVE
I, 1974, 167-179.
ATTENTION,
AND THE EVOKED ROBERT Medical U.K.
Council,
Accepted for publication
CONTINGENT
Publishing
NEGATIVE
Company
VARIATION
POTENTIAL
T. WILKINSON Research
@ North-Holland
and SUSAN Applied
M. ASHBY
Psychology
Unit (Annexe),
Cambridge
CB2 2BW,
28 June 1973
Contingent negative variation (CNV), Nl-P2 amplitude of the evoked potential (EP), and positivity at 300, 400 and 500 msec latency (P300, P400 and PSOO) were measured in relation to task relevant (R) or irrelevant (I) tones presented alternately or unpredictablv at 1 set intervals. High concordance of P300, 400 and 500 indicated a slow. relatively unpeaked wave thought to be the CNV resolution. Both Nl-P2 and P300 appeared small only when stimuli were both irrelevant and predictably so. With predictable presentation correlations were observed between CNV, Nl-P2 and P300 in terms of both absolute level and, particularly, relevantiirrelevant difference. Holding CNV constant statistically, and to a lesser extent P300, reduced these correlations. It is suggested that CNV resolution in the post-stimulus trace reflects selective attention paid to the stimulus, and may be responsible, through summation, for claims that Nl-P2, and sometimes P300, does so.
1. Introduction As a result of a series of experiments carried out some years ago, Naatlnen (1967) concluded that the average evoked potential (EP) recorded from the scalp at the vertex reflected selective attention in predictable settings, where subjects knew when stimuli would occur, but not in unpredictable ones where they did not. In considering the possible contribution of slow potential changes to this result, NBltSinen reported that contingent negative variation (CNV) was present in the predictable setting and returned to baseline following relevant but not irrelevant stimuli. In passing he also noted that the subjects with the larger CNVs tended to show greater effects of selective attention upon the EP. Although NaatHnen took measurements upon a number of components in the EP, his main conclusions related to the prominent wave composed of a negative deflection (Nl) at about 110 msec followed by a positive one (P2) at about 170 msec. The implication of these results are thought to be important enough to warrant a replication of his study, but with certain additions and changes. First, NMtanen’s settings of predictable and unpredictable presentation of the relevant and irrelevant stimuli differed in certain other important respects, in particular the kind of stimuli used and the average inter-stimulus interval. 167
168
R. T. Wilkinson
and S. M. Ashby
The variable of predictability can be better assessed if these are held constant. Second, conventional significance levels were not adduced for at least two of the more important claims; these need to be achieved if possible. Third, if the results obtained by Naatanen are replicated they merit discussion in light of what has been found during the six years which have elapsed since the publication of his stimulating monograph. 2. Method Eight subjects took part, attending for one session only. The records of one were excluded from analysis as clear evoked potentials could not be observed. Following practice in what was required they carried out an experimental session as follows. They were asked to listen to two tones 10 msec in duration, presented at 1 set intervals, and of frequency either 400 or 1500 Hz. In the predictable condition the high and low tones alternated; in the unpredictable condition they occurred in a quasi-random order which greatly reduced the subject’s ability to predict the onset of relevant stimuli. Eight runs having 40 high and 40 low tones in each were presented. The subject’s task was to listen to one of the tones, designated relevant (R), for the occasional ‘signal tone’, this being a tone amongst a series which was longer (40 msec) than the rest. This was a relatively easy discrimination giving rise to few errors either of omission or commission. The other irrelevant (I) tones could be ignored. In some runs the high tone was designated relevant and in others the low. In each run there were eight signal tones distributed irregularly in time. The subjects recorded their detection of a signal by pressing a button. Of the eight runs presented, half were in the predictable and half in the unpredictable conditions, and these halves were again divided equally on the basis of making either the high or the low tone the relevant channel which contained the signals. The tone that was designated irrelevant contained no signals in that run. The order of presentation of predictable and unpredictable conditions and high or low tone relevancy was balanced over the group of subjects on an ABBA basis for the former and AABB for the latter. In statistical analysis, except where stated otherwise, differences between means are tested by Wilcoxon’s procedure (Siegel, 1956). The EEG was derived from an Ag-AgCl electrode at the vertex and a similar electrode on one of the mastoid processes. The subject was earthed by an electrode on the other mastoid process. The EEG was amplified by a Grass 7Pl pre-amplifier and a 7DAC driver unit. The points at which the frequency response of the system fell to half full amplitude were 75 and 0.1 Hz. The output of this system was recorded on-line on magnetic tape for subsequent off-line response averaging by a computer of average transients. To control for contamination of the EEG record by eye movements the subjects were required to fixate a point 60 cm directly in front of them (Hillyard and Galambos, 1970) and to refrain from blinking at or shortly
Attention, CNV, and evoked potential
169
after the onset of stimuli. They were watched closely throughout the test to see that they complied with these instructions. As a check the EOG was recorded from the upper and lower canthus of the left eye and averaged at the same time as the EEG. For the most part the EOGs were essentially flat and such variation as appeared was unrelated to the observed changes in EP and CNV in response to the experimental variables. 3. Results 3.1. ~t~~u~~
relevance in ~redictabie and unpred~ctab~e c~nditi~ns
Evoked potentials were averaged separately for the R and I stimuli in the predictable and unpredictable conditions. All signal stimuIi were excluded from the average. Thus the number of samples for each EP was 32, being derived from each of the four runs in either the predictable or unpredictable condition. The computer was triggered by the appropriate pulses recorded 200 msec before each kind of stimulus. A measure was taken of the peak-topeak amplitude of the prominent deflection of the basic EP having a negative peak (Nl) about 110 msec post-stimulus and a positive peak (P2) about 170 msec post-stimulus. Following convention this wave is referred to as Nl-P2. The average over all subjects of Nl-P2 in the predictable condition was 10.0 PV following R stimuli and 8.4 FV following I. The difference between these two was significant (p (0.05) on a sign test. Corresponding measures taken from the traces of the unpredictable runs were R: 10.4 FV, and I: 10.6 pV. The difference between these two was not itself significant and was smaller than that of the corresponding difference in the predictable condition, this interaction being significant (p ~0.05). Considering now the influence of stimulus predictability, Nl-P2 was larger for unpredictable than for predictable presentation (p (0.02) but, reflecting the above interaction, the effect was confined mainly to the I stimuli. The positivity of the traces relative to the EEG level at stimulus onset was measured at a point 300 msec post-stimulus. This measure is sometimes referred to as P3 (Wilkinson and Morlock, 1967; Tueting, Sutton and Zubin, 1971). In other papers (Donch~n and Cohen, 1967; Hillyard, Squires, Bauer and Lindsay, 1971) it is termed P300, a name we wiI1adopt for reasons which will become clear later. With predictable presentation the amplitude of P300 was higher for R (3.0 pV) than for I (1.38 pV) stimuli. For unpredictable presentation its amplitude was lower for R (2.9 FV) than for I (4.2 pV) stimuli. Neither of these differences reached significance but the interaction between relevance and predictability did (p ~0.05): as with Nl-P2, P300 was larger with unpredictable than with predictable presentation in the case of I tones (p ~0.01) but with R tones there was little difference. 3.2. Analysis of multi-st~muius traces in the predictable condition Figure 1 shows these traces averaged over periods of 4 set in the predictable
170
R. T. Wilkinson
I
SUBJECT BE
and S. M. Ashbr
R
I
R
-P
FO
MI
ONSET OF STIMULI EITHER RELEVANT OR IRRELEVANT
(R)
(I)
4 sec. Fig. 1. Averaged EEG traces of 4 set duration for each subject. The traces are triggered by pulses 200 msec before the irrelevant stimulus and are confined tc the alternating, predictable mode of presentation. Each trace thus contains EPs to relevant (R) and irrelevant (I) stimuli in the order IRIR and at 1 set intervals with CNVs, when present. developing in the intervals between the EPs and prior to stimulus onset. An upward deflection of the trace indicates negativity at the active electrode.
condition for each subject. To obtain these averages the computer scan of the EEG was initiated by a trigger which preceded the I tone by 200 msec. The
Attention,
CN V, and evoked potential
171
4 set scan which followed thus encompassed four stimuli in the order IRIR and terminated 790 msec after the last of these stimuli. The computer then accepted the next I trigger (due 10 msec after the end of the previous scan) to initiate the second four-stimulus scan, and so on. Occasionally this acceptance had to be delayed to exclude signal stimuli from the traces. This reduced the number of samples to 16/average. As I and R stimuli alternated in the predictable condition, the EPs to the I and R stimuli, and also the CNVs preceding them, accumulated at the same points along the trace. These R and I stimulus onset points are shown in fig. 1. In the case of all subjects clear EPs can be seen to the tones occurring at 200, 1200,220O and 3200 msec along the trace. In most subjects CNVs precede the R but not the I stimuli. An arbitrary baseline was drawn roughly by eye to divide the traces shown in fig. 1 into equal positive and negative areas. The negative ampltude of CNV was measured above the baseline at the point of stimulus onset. Average CNV was larger preceding R stimuli (3.9 pV) than I stimuli (0.6 pV) in the predictable runs, the difference between the two being significant (p ~0.05). A similar comparison based on 4 set traces cannot, of course, be made for the unpredictable runs due to the random order of the tones. In light of what has been said in the literature (e.g. Tueting and Sutton, 1973) concerning the significance of the P3 or P300 component, a search was made for convincing evidence of a discrete wave at this point in our records. None was revealed. In the 4 set traces (fig. 1), however, there were signs of a much slower positive wave in the EEG extending from about 200-500 msec post-stimulus. Therefore, as well as taking the conventional measure of P300, namely positivity at a latency 300 msec relative to that at the stimulus onset, the same measure was taken at latency 400 and 500 msec. In the 4 set records of the predictable runs R minus I differences were positive in all seven subjects for the P300 measure (p
and partial correlations
between
CNV, Nl-P2,
172
R. T. Wilkinson and S. M. Ashby
fable 1. Product-moment correlations and partial correlations between CNV, P300, 400, 500 and Nl-P2. Correlations significant at p co.05 are indicated by an asterisk, p co.01 by a double asterisk. Correlation Terms correlated
Absolute scores predictable condition Relevant stimuli
CNV vs. P3OO CNV vs. P400 CNV vs. PSOO Nl-P2 vs. CNV Nl-P2 vs. P300 CNV vs. P300 (Nl-P2 constant) N1-P2 vs. CNV (P300 constant) Nl-P2 vs. P300 (CNV constant)
Relevantirrelevant score
Irrelevant stimuli
-i-0.78*
+0.35
+0.70 -to.43 +0.74 +-OS7 -0.26
-0.06 -0.09 +0.35 -0.03 -0.07
+0.89** +0.80* +0.85** +0.90** +0.79* +0.67 +0.67 -0.05
and P300 (and in some cases P400 and P500) are shown in table 1. All measures were taken from the 4 set traces of the predictable condition and are in terms of either absolute level or selective attention effect (relevant minus irrelevant amplitude). The correlation between CNV and P300 was high for relevant tones but substantially less for irrelevant stimuli. Holding N l-P2 constant produced almost no change in these correlations. Correlations between Nl-N2 and the other two measures, CNV and P300, were lower and holding each of these constant substantially reduced the partial correlation of Nl-P2 with the other. In terms of selective attention effect (relevant minus irrelevant amplitude) the correlations between all three pairings of CNV, Nl-P2 and P300 were high and only seriously reduced when CNV was held constant. Finally it seemed to make little difference to the correlation levels whether the positive-going wave ‘P300’ was measured at latency 300,400 (P400), or 500 msec (P500).
4. Discussion A consensus of EP studies of selective attention suggests that the peak-to-peak amplitude of the EP from a negative deflection (Nl) at about I10 msec to a positive deflection (P2) at about 170 msec is larger following relevant, as compared with irrelevant, stimuli in behavioural situations calling for the exercise of selective attention, but only when that situation is predictable in that the subject knows roughly when a relevant or irrelevant stimulus will occur (Chapman and Bragdon, 1964; Davis, 1964; Spong, Haider and Lindsley, 1965 ; Debecker and Desmedt, 1966; Rietveld, Tordoir and Hagenouw, 1966; Naatanen, 1967 (Exp. III); Shea& and Chapman, 1969). Where relevant and irrelevant stimuli occur in random order and at random intervals of not less than 1 set it is found, with but one exception (Eason,
Attention,
CN V, and evoked potential
173
Harter and White, 1969), that Nl-P2 is the same for both relevant and irrelevant stimuli (Donchin and Cohen, 1967; NaiBtanen, 1967 (Exp. II); Smith, Donchin, Cohen and Starr, 1970; Hartley, 1970; Karlin, Martz and Mordkoff, 1970). Since in practice we appear as capable of attending to random stimuli as to alternating stimuli these latter results have discouraged the view that the amplitude of the main N-P2 wave of the EP can indicate in any general way that selective attention is being paid to the stimulus concerned. However, in none of the experiments cited above has it been possible to make direct comparison between alternating and random modes of presentation. Usually these contrasting forms of the test have appeared in different experiments with other factors varying as well. One purpose of the present study was to make such a direct comparison by giving predictable and unpredictable forms of the test to the same subjects. The outcome has been that previous findings have been confirmed. The EP was larger for relevant stimuli than for irrelevant stimuli with alternating presentation but not with random order presentation. Comparisions within subjects were able to reveal that the absence of a relevant/irrelevant difference with unpredictable presentation was because both stimuli produced EPs of high amplitude equal to that of the relevant stimuli in the predictable alternating setting. This suggests a solution to the problem of why the effect fails to appear when relevant and irrelevant stimuli occur unpredictably: both stimuli are effectively relevant as far as the EP is concerned merely because the onset of either one presents task-relevant information. With alternating presentation no task-relevant information is passed when a predictably irrelevant stimulus occurs at a predictable point in time. It was to solve the problem of the absence of relevant/irrelevant difference with unpredictable presentation that Naatanen (1967, 1970) used longer time constant recordings which permitted CNVs to appear in the records of his condition in which relevant and irrelevant stimuli alternated. He found, as we have, that CNVs were present before relevant but not before irrelevant stimuli. We have also shown that the relevant/irrelevant difference in the EP amplitude correlated across subjects with the degree to which the CNV at the point of relevant stimulus onset exceeded that at the point of irrelevant stimulus onset. Paradoxically, this aspect of our results provides support for Naatanen’s (1967) suggestion that the EP, far from reflecting stimulus relevance, is a function merely of the amplitude of the CNV upon which the stimulus impinges, the CNV itself reflecting the level of cortical activation. The question remains then, does the main Nl-P2 component of the auditory EP reflect selective attention, or if not why does it appear to do so in many experiments ? Before examining the question further it may be helpful to consider the
174
R. T. Wilkinson
and S. M. A&b?’
behaviour of the late positive wave which we call, for convenience, but without prejudice, P300. It is difficult to know whether this is the same corn. ponent that has been referred to as the ‘late positive component’ by SuttonBraren, Zubin and John (1965), ‘P3’ by Wilkinson and Morlock (1967). or ‘P300’ by Hillyard et al. (1971). In the present records it certainly was not a sharp transient wave like those waves whose amplitude Wilkinson and Morlock found to be related to reaction time. Hovvever, there are other authors whose studies have presented pictures of broad vvav’es similar to those reported here and who have referred to them as ‘P3’ or ‘P300’. Such waves have been claimed to vary in amplitude with stimulus probability or uncertainty (Sutton et al., 1965; Sutton. Tueting, Zubin and John, 1966: Tueting et al., 1971). relevance (Donchin and Smith, 1970; Sheatz and Chapman, 1969; Wilkinson and Lee, 1972). and both discriminability (Hillyard et al., 1971) and response criterion (Paul and Sutton. 1972) in auditory signal detection. It is important in this context to distinguish clearly between P300 and the main Nl-P2 component of the EP. Unlike Nl-P2, which is highly stimulus bound, a P300 wave can appear with no stimulus delivery at all if the stimulus is expected at a particular point in time (Barlow, Morrell and Morrell. 1965; Sutton et al., 1966: Klinke. Fruhstorfer and Finenzeller, 1968). This P300 has the same spatial distribution about the cortex and the same temporal relationship to the overt motor response as the P300 wave which may follow a stimulus (Picton, Hillyard and Galambos, in press). On the other hand, Wilkinson and Morlock (1967) showed that their P3 vanished completely from the post-stimulus trace when no reaction time responses were made to their stimuli, whereas the Nl-P2 wave is always present when a stimulus occurs, albeit perhaps at reduced amplitude if the stimulus intensity is low. In the present data P300, as defined here, reflected both stimulus relevance and stimulus unpredictability, but in no simple way: it was larger with relevant stimuli, but only with predictable presentation and then only significantly so in the 4 set traces. It was larger with unpredictable stimuli, but only vvhen they were irrelevant. This simplifies to the fact that, as with Nl-P?, P300 was small when stimuli were predictably irrelevant. This is in general agreement with the current view that positivity at 300 msec post-stimulus reflects the degree to which a slimulus resolves uncertainty (see Tueting and Sutton. 1973, for review). NBatanen (1967) has shown that any CNV which is present at stimulus onset may be returned to baseline if the stimulus is a relevant one as compared with an irrelevant one. The effect has been confirmed by Wilkinson and Lee (1972). In all of these experiments the nature of the relevant stimulus was such as to resolve uncertainty, usually related to signal detection, in a way which the irrelevant stimulus could not. This, coupled with the claim that the amplitude of P300 waves also reflects stimulus uncertainty. suggests that
Artenrion,
CN V, and evoked potential
175
there is an association between the two processes, CNV and P300. The most parsimonious suggestion is that they constitute the same process. In other words, P300 is the return of CNV to baseline (Donchin and Cohen, 1967; Donchin and Smith, 1970) and is only positive in relation to the negative level (CNV) of the EEG at the point of stimulus onset. It is a positive-going return to zero which may overshoot baseline and be peaked in a manner resembling a transient component when recordings are made with relatively short time constants. Another version of the association is that the CNV return modulates the amplitude of an existing P300 wave produced directly by the stimulus (Karlin, 1970). A third version is that changes in P300 are due to a heightened level of cortical activation of which CNV is just another sign (Naatanen, 1967, 1969). Various authors have attempted to assess the validity of these suggestions by relating the level of CNV at stimulus onset to the amplitude of P300 (Lombroso, 1970; Donchin and Smith, 1970; Small and Small, 1970; Donchin, Gerbrandt, Leiffer and Tucker, 1972) though none actually correlate the two. In general these studies fail to agree, some suggesting a relationship and some not. In this study the correlation between absolute level of CNV and P300 was relatively high for relevant stimuli (+0.78) but much lower for irrelevant ones (+0.35). This again suggests that the relationship depends not just upon the pre-stimulus level of CNV but also upon whether the stimulus is more (relevant) or less (irrelevant) likely to cause CNV to return to baseline. In many of the earlier studies which examined the CNV/P300 association there were differences between stimuli either within or between conditions which would be expected to influence their relevance and consequently, on the present hypothesis, their ability to return any CNV that was present to baseline. To the extent that the latter may influence positivity at 300 msec we would not necessarily expect prior CNV level alone to correlate with P300 except under conditions where stimulus relevance is kept reasonably constant or the parameter is the difference between relevant and irrelevant stimuli. Where these conditions have been met in the present study the correlations between prior CNV and P300 have been substantial and significant. Furthermore these correlations were maintained when the positive-going wave was sampled at 400 and 500 msec latency. This shows that the effects observed cannot have been due to the variation of some late component of the EP itself at around 300 msec latency due either to its summation with the CNV resolution (Karlin, 1970) or to that component being augmented in some way by the heightened cortical excitation which Naatanen (1967, 1970) suggests is the concomitant of CNV. Thus the present data support, and previous data do not effectively discount, the view that the kind of slow positive or P300 waves we have recorded constitute the reactive return of CNV to baseline as reproduced by the typical finite time constant recording system. The same may be true for
176
R. T. Wilkinson
and S. M. Ashby
some of the longer and less transient P300 waves reported elsewhere and even shallower ones when time constants are short. Given then, that a CNV is present in the first place, if it can be accepted that the triggering of its return and the latency of that process depends upon the relevance, uncertainty, discriminability, or motivational importance of the stimulus, many of the empirical results concerning P300 become easier to explain. This may be done either on the basis of CNV return being confused with a discrete P3 wave of the EP or, more probably, of a selectively triggered CNV resolution summating with an existing P3. Before resting this case, however, a study by Donald and Goff (1971) should be considered. These authors, aware of the possibility that both prior CNV and the ability to return CNV to baseline might contribute to the CNV/P300 relationship, attempted to control both. Following a warning stimulus their subjects received a shock which was either relevant or not relevant to the task of making a choice response to a third and final stimulus. CNV level at the onset of the second, shock stimulus was controlled by selecting traces which contained the same CNV deviation from baseline. An attempt was made to control CNV return by requiring subjects to delay an overt response to the shock stimulus until the arrival of the third choice response stimulus some 500-1500 msec later. In spite of the controls they observed variations in P300 as a function of the relevance of the shock stimulus, and thus they claimed to have proved a dissociation between CNV and P300. However, praiseworthy as this attempt is, it is not wholly convincing. CNV can develop as soon as 200400 msec following a warning stimulus (Posner and Wilkinson, 1969; Rebert and Knott, 1970) if the interstimulus interval between warning and imperative stimulus is reasonably short. It seems quite possible that the CNV before the second, shock stimulus may in fact have returned towards baseline and then redeveloped rapidly in preparation for the third stimulus to which a response had to be made, as found by Wilkinson and Spence (1973). Unfortunately, the rather large EPs to the shock make it difficult to be sure of this from examination of the traces shown by Donald and Goff. Replication using a weak stimulus at this point would be desirable, but meanwhile it seems doubtful whether this study provides sufficient evidence to reject the view that CNV and P300 are associated, or indeed that the slow positive-going wave observed in the present study and in a number of others constitutes the return of CNV to baseline and is not a potential evoked directly by the stimulus, as Nl-P2 seems to be. We return now to our main concern, a decision as to whether Nl-P2 does or does not reflect selective attention. Although there have been suggestions that the return of CNV to baseline may summate with a discrete P3 wave in the EP (Karlin, 1970), the earlier Nl-P2 wave has been neglected in this respect, except for the early work of Naatanen (1967), presumably because it was thought that the CNV could not return quickly enough to summate
Attention, CN V, and evoked potential
177
of the EP. An inspection of the traces in fig. 1 strongly suggests that it can. These phenomena support the proposition made by Wilkinson and Lee (1972) that Nl-P2 appears to reflect selective attention because it summates with the CNV return following selectively upon relevant stimuli. These authors argued that the positive-going CNV return was the true feature of the post-stimulus trace to reflect selective attention because its amplitude was related to selective attention performance, whereas that of Nl-P2 was not. It was unfortunate that Wilkinson and Lee were unable to average the pre-stimulus EEG and thus observe the presence of prior CNV rather than infer it. In the present study the omission was rectified. In fig. 1, CNVs can be seen preceding the relevant stimulus, returning to baseline with its onset, and summating with the Nl-P2 wave in such a way as to make it appear amplified following relevant, as compared with irrelevant, stimuli. Other traces can be found in the CNV literature showing the same effect, for example during the vigilance task used by Wilkinson and Haines (1970, see fig. la, especially subject 2). If earlier arguments can be accepted that the present late positive wave (P300-500) represents the extent of CNV return to baseline, the Wilkinson and Lee proposal is supported empirically by the high correlations between pre-stimulus CNV, P300, 400, 500 and Nl-P2 in the degree to which they reflected relevant/irrelevant differences. To summarise, therefore, it is suggested that two factors, (1) stimulus onset CNV level, and (2) ability of the stimulus to return CNV to baseline, decide the amplitude of ‘Nl-P2’ as a function of selective attention. To derive further support for this general proposition we may consider the correlations and partial correlations between the present CNV, P300 and Nl-P2 in terms of absolute levels and amplitudes for stimuli in the predictable condition (table 1). For both relevant and irrelevant stimuli the correlation between CNV and P300 remained virtually unchanged when Nl-P2 was held constant, indicating that Nl-P2 was not influencing these two measures. On the other hand, holding either CNV or P300 constant reduced the correlation of Nl-P2 with the other, suggesting again that CNV at stimulus onset and the degree of CNV resolution by the stimulus (as indicated by the present P300 measure) are the true determinants of the amplitude of Nl-P2 as selective attention is varied.
with this component
References Barlow, J. S., Morrell, L. and Morrell, F. (1965). On evoked responses
in relation to temporal conditioning to paired stimuli in man. MIT. Research Laboratories Electronic Quarterly Progress Report, 78, 263-272. Chapman, R. M. and Bragdon, H. R. (1964). Evoked response to numerical and nonnumerical stimuli while problem solving. Nature (London), 203, 1155-1157. Davis, H. (1964). Enhancement of evoked cortical potentials in humans related to tasks requiring a decision. Science, 145, 182-183. Debecker, J. and Desmedt, J. E. (1966). Rate of intermodality switching disclosed by
R. T. Wilkinson and S. M. Ashby
178
sensory evoked potentials averaged during signal detection tasks. Journal of Phy.siology (London), 185, 52-53. Donald, M. W. and Gaff, W. R. (1971). Attention-related increases in cortical responsivity, dissociated from the contingent negative variation. Science, 172, 1163-1166. Donchin, E. and Cohen, L. (1967). Averaged evoked potentials and intra-modality selective attention. Electroencephalography and Clinical Neurophysiology, 22, 537-546. Donchin, E., Gerbrandt, L. A., Leiffer, L. and Tucker, L. (1972). Is the contingent negative variation a motor response? Psychophysiology, 9, 178-l 79. Donchin, E. and Smith, D. B. D. (1970). The contingent negative variation and the late positive wave of the average evoked potential. Electroencephalography and Clinical Neurophysiology,
29, 201-203.
Eason, R. G., Harter, M. R. and White, C. T. (1969). Effects of attention and arousal on visually evoked cortical potentials and reaction time in man. Physiological Behaviour,
4, 283-289.
Gilden, L., Vaughan, H. G. and Costa, L. D. (1966). Summated human EEG potentials with voluntary movement. Electroencephalography arrd Clinical Neurophysiology, 20, 433-438.
Hartley, L. R. (1970). The effect of stimulus relevance on the cortical evoked potentials. Quarterly Journal of Experimental
Hillyard,
S. A. and Galambos,
encephalography
Psychology,
22, 531-546.
R. (1970). Eye movement
and Clinical Neurophysiology,
artefact in the CNV. Electro-
28, 173- 182.
Hillyard, S. A., Squires, K. C., Bauer, J. W. and Lindsay, P. H. (1971). Evoked potential correlates of auditory signal detection. Science, 172, 1357-1360. Karlin, L. (1970). Cognition, preparation and sensory evoked potentials. Psychological Bulletin, 73, 122-136.
Karlin, L., Martz, M. J. and Mordkoff, A. M. (1970). Motor performance and sensory evoked potentials. Electroencephalography and Clinical Neurophysiology,, 28, 307-3 13. Klinke, R., Fruhstorfer, H. and Finenzeller, P. (1968). Evoked responses as a function of external and stored information. Electroencephalowaphv and Clinical Neurophysiology,
25, 119-I 22.
Lombroso, C. T. (1970). The CNV during tasks requiring choice. In: Evans, C. R. and Mulholland. T. B. (Eds.) Attention in Neurophysiology. Butterworth: London. 64-69. Naatanen, R. (1967). Selective attention and evoked potentials. Anna/es Academiae Scientiarum
Naatanen,
Fennicae,
25, l-226.
R. (1969). Anticipation
of relevant stimuli and evoked potentials.
Perceptual
and Motor Skills, 28, 639-646.
Naatanen. R. (1970). Evoked potential. EEG and slow potential correlates of selective attention. In: Sanders, A. F. (Ed.) Attention and Performance III, Acta Psychologica. North-Holland: Amsterdam, 178-192. Paul, D. D. and Sutton, S. (1972). Evoked potential correlates of response criterion in auditory signal detection. Science, 177, 362-364. Picton, T. W., Hillyard, S. A. and Galambos, R. (In press). Cortical evoked responses to omitted stimuli. In: Livanov, M. N. (Ed.) MajorProblemsofBrain Electrophysiology. U.S.S.R. Academy of Sciences. Posner, M. I. and Wilkinson, R. T. (1969). On theprocess ofpreparation. Paper presented to Psychonomic Society (USA), Nov. 1969. Rebert, C. S. and Knott, J. R. (1970). The vertex non-specific potential and latency of contingent negative variation. Electroencephalography and Clinical Neurophysiology, 28, 561-565.
Reitveld, W. J., Tordoir, W. E. M. and Hagenouw, J. R. B. (1966). Influence of attentiveness, of vigilance task difficulty and of habituation on cortical evoked responses and on artefacts. Acta Physiologica et Pharmacologica Neerlandica, 14, 18-37. Sheatz, G. C. and Chapman, R. M. (1969). Task relevance and auditory evoked responses. Electroencephalography
and Clinical Neurophysiology,
26, 468-475.
Siegel, S. (1956). Nonparametric Statistics. McGraw-Hill: New York. Small, J. G. and Small, I. F. (1970). Interrelationships of evoked and slow potential responses. Diseases of the Nervous System, 31, 459-464.
Attention,
CN V, and evoked potential
179
Smith, D. B. D., Donchin, E., Cohen, L. and Starr, A. (1970). Auditory averaged evoked potentials in man during selective binaural listening. EIectroencephalographv and Clinical Neurophysiology,
28, 146-152.
Spong, P., Haider, M. and Lindsley, D. B. (1965). Selective attentiveness and cortical evoked response to visual and auditory stimuli. Science, 148, 395-397. Sutton, S., Braren, M., &bin, J. and John, E. R. (1965). Evoked potential correlates of stimulus uncertainty. Science, 150,1187-l 188. Sutton, S., Tueting, P., Zubin, J. and John, E. R. (1966). Information delivery and the sensory evoked potential. Science, 155, 1436-1439. Tueting, P. and Sutton, S. (1973). In: Kornblum, S. (Ed.) Attention and Performance. Academic Press: New York. Tueting. P.. Sutton. S. and Zubin, J. (1971). Quantitative evoked potential correlates of the probability of events. Psychophysio;ogyt 7, 385-394. _ Wilkinson, R. T. and Haines, E. (1970). Evoked response correlates of expectancy during vigilance. Acta Psychologica, 33, 402-413. Wilkinson, R. T. and Lee, M. V. (1972). Auditory evoked potentials and selective attention. Electroencephalography and Clinical Neurophysiology, 33, 41 l-41 8. Wilkinson, R. T. and Morlock, H. C. (1967). Auditory evoked response and reaction time. Eiectroencephalography and Clinical Neurophysiology, 23, 50-56. Wilkinson, R. T. and Spence, M. T. (1973). Determinants of the post-stimulus resolution of contingent negative variation (CNV). Electroencephalography and Clinical Neurophysiology,
35, 503-509.
Psychology,
SELECTlVE
I, 1974, 167-179.
ATTENTION,
AND THE EVOKED ROBERT Medical U.K.
Council,
Accepted for publication
CONTINGENT
Publishing
NEGATIVE
Company
VARIATION
POTENTIAL
T. WILKINSON Research
@ North-Holland
and SUSAN Applied
M. ASHBY
Psychology
Unit (Annexe),
Cambridge
CB2 2BW,
28 June 1973
Contingent negative variation (CNV), Nl-P2 amplitude of the evoked potential (EP), and positivity at 300, 400 and 500 msec latency (P300, P400 and PSOO) were measured in relation to task relevant (R) or irrelevant (I) tones presented alternately or unpredictablv at 1 set intervals. High concordance of P300, 400 and 500 indicated a slow. relatively unpeaked wave thought to be the CNV resolution. Both Nl-P2 and P300 appeared small only when stimuli were both irrelevant and predictably so. With predictable presentation correlations were observed between CNV, Nl-P2 and P300 in terms of both absolute level and, particularly, relevantiirrelevant difference. Holding CNV constant statistically, and to a lesser extent P300, reduced these correlations. It is suggested that CNV resolution in the post-stimulus trace reflects selective attention paid to the stimulus, and may be responsible, through summation, for claims that Nl-P2, and sometimes P300, does so.
1. Introduction As a result of a series of experiments carried out some years ago, Naatlnen (1967) concluded that the average evoked potential (EP) recorded from the scalp at the vertex reflected selective attention in predictable settings, where subjects knew when stimuli would occur, but not in unpredictable ones where they did not. In considering the possible contribution of slow potential changes to this result, NBltSinen reported that contingent negative variation (CNV) was present in the predictable setting and returned to baseline following relevant but not irrelevant stimuli. In passing he also noted that the subjects with the larger CNVs tended to show greater effects of selective attention upon the EP. Although NaatHnen took measurements upon a number of components in the EP, his main conclusions related to the prominent wave composed of a negative deflection (Nl) at about 110 msec followed by a positive one (P2) at about 170 msec. The implication of these results are thought to be important enough to warrant a replication of his study, but with certain additions and changes. First, NMtanen’s settings of predictable and unpredictable presentation of the relevant and irrelevant stimuli differed in certain other important respects, in particular the kind of stimuli used and the average inter-stimulus interval. 167
168
R. T. Wilkinson
and S. M. Ashby
The variable of predictability can be better assessed if these are held constant. Second, conventional significance levels were not adduced for at least two of the more important claims; these need to be achieved if possible. Third, if the results obtained by Naatanen are replicated they merit discussion in light of what has been found during the six years which have elapsed since the publication of his stimulating monograph. 2. Method Eight subjects took part, attending for one session only. The records of one were excluded from analysis as clear evoked potentials could not be observed. Following practice in what was required they carried out an experimental session as follows. They were asked to listen to two tones 10 msec in duration, presented at 1 set intervals, and of frequency either 400 or 1500 Hz. In the predictable condition the high and low tones alternated; in the unpredictable condition they occurred in a quasi-random order which greatly reduced the subject’s ability to predict the onset of relevant stimuli. Eight runs having 40 high and 40 low tones in each were presented. The subject’s task was to listen to one of the tones, designated relevant (R), for the occasional ‘signal tone’, this being a tone amongst a series which was longer (40 msec) than the rest. This was a relatively easy discrimination giving rise to few errors either of omission or commission. The other irrelevant (I) tones could be ignored. In some runs the high tone was designated relevant and in others the low. In each run there were eight signal tones distributed irregularly in time. The subjects recorded their detection of a signal by pressing a button. Of the eight runs presented, half were in the predictable and half in the unpredictable conditions, and these halves were again divided equally on the basis of making either the high or the low tone the relevant channel which contained the signals. The tone that was designated irrelevant contained no signals in that run. The order of presentation of predictable and unpredictable conditions and high or low tone relevancy was balanced over the group of subjects on an ABBA basis for the former and AABB for the latter. In statistical analysis, except where stated otherwise, differences between means are tested by Wilcoxon’s procedure (Siegel, 1956). The EEG was derived from an Ag-AgCl electrode at the vertex and a similar electrode on one of the mastoid processes. The subject was earthed by an electrode on the other mastoid process. The EEG was amplified by a Grass 7Pl pre-amplifier and a 7DAC driver unit. The points at which the frequency response of the system fell to half full amplitude were 75 and 0.1 Hz. The output of this system was recorded on-line on magnetic tape for subsequent off-line response averaging by a computer of average transients. To control for contamination of the EEG record by eye movements the subjects were required to fixate a point 60 cm directly in front of them (Hillyard and Galambos, 1970) and to refrain from blinking at or shortly
Attention, CNV, and evoked potential
169
after the onset of stimuli. They were watched closely throughout the test to see that they complied with these instructions. As a check the EOG was recorded from the upper and lower canthus of the left eye and averaged at the same time as the EEG. For the most part the EOGs were essentially flat and such variation as appeared was unrelated to the observed changes in EP and CNV in response to the experimental variables. 3. Results 3.1. ~t~~u~~
relevance in ~redictabie and unpred~ctab~e c~nditi~ns
Evoked potentials were averaged separately for the R and I stimuli in the predictable and unpredictable conditions. All signal stimuIi were excluded from the average. Thus the number of samples for each EP was 32, being derived from each of the four runs in either the predictable or unpredictable condition. The computer was triggered by the appropriate pulses recorded 200 msec before each kind of stimulus. A measure was taken of the peak-topeak amplitude of the prominent deflection of the basic EP having a negative peak (Nl) about 110 msec post-stimulus and a positive peak (P2) about 170 msec post-stimulus. Following convention this wave is referred to as Nl-P2. The average over all subjects of Nl-P2 in the predictable condition was 10.0 PV following R stimuli and 8.4 FV following I. The difference between these two was significant (p (0.05) on a sign test. Corresponding measures taken from the traces of the unpredictable runs were R: 10.4 FV, and I: 10.6 pV. The difference between these two was not itself significant and was smaller than that of the corresponding difference in the predictable condition, this interaction being significant (p ~0.05). Considering now the influence of stimulus predictability, Nl-P2 was larger for unpredictable than for predictable presentation (p (0.02) but, reflecting the above interaction, the effect was confined mainly to the I stimuli. The positivity of the traces relative to the EEG level at stimulus onset was measured at a point 300 msec post-stimulus. This measure is sometimes referred to as P3 (Wilkinson and Morlock, 1967; Tueting, Sutton and Zubin, 1971). In other papers (Donch~n and Cohen, 1967; Hillyard, Squires, Bauer and Lindsay, 1971) it is termed P300, a name we wiI1adopt for reasons which will become clear later. With predictable presentation the amplitude of P300 was higher for R (3.0 pV) than for I (1.38 pV) stimuli. For unpredictable presentation its amplitude was lower for R (2.9 FV) than for I (4.2 pV) stimuli. Neither of these differences reached significance but the interaction between relevance and predictability did (p ~0.05): as with Nl-P2, P300 was larger with unpredictable than with predictable presentation in the case of I tones (p ~0.01) but with R tones there was little difference. 3.2. Analysis of multi-st~muius traces in the predictable condition Figure 1 shows these traces averaged over periods of 4 set in the predictable
170
R. T. Wilkinson
I
SUBJECT BE
and S. M. Ashbr
R
I
R
-P
FO
MI
ONSET OF STIMULI EITHER RELEVANT OR IRRELEVANT
(R)
(I)
4 sec. Fig. 1. Averaged EEG traces of 4 set duration for each subject. The traces are triggered by pulses 200 msec before the irrelevant stimulus and are confined tc the alternating, predictable mode of presentation. Each trace thus contains EPs to relevant (R) and irrelevant (I) stimuli in the order IRIR and at 1 set intervals with CNVs, when present. developing in the intervals between the EPs and prior to stimulus onset. An upward deflection of the trace indicates negativity at the active electrode.
condition for each subject. To obtain these averages the computer scan of the EEG was initiated by a trigger which preceded the I tone by 200 msec. The
Attention,
CN V, and evoked potential
171
4 set scan which followed thus encompassed four stimuli in the order IRIR and terminated 790 msec after the last of these stimuli. The computer then accepted the next I trigger (due 10 msec after the end of the previous scan) to initiate the second four-stimulus scan, and so on. Occasionally this acceptance had to be delayed to exclude signal stimuli from the traces. This reduced the number of samples to 16/average. As I and R stimuli alternated in the predictable condition, the EPs to the I and R stimuli, and also the CNVs preceding them, accumulated at the same points along the trace. These R and I stimulus onset points are shown in fig. 1. In the case of all subjects clear EPs can be seen to the tones occurring at 200, 1200,220O and 3200 msec along the trace. In most subjects CNVs precede the R but not the I stimuli. An arbitrary baseline was drawn roughly by eye to divide the traces shown in fig. 1 into equal positive and negative areas. The negative ampltude of CNV was measured above the baseline at the point of stimulus onset. Average CNV was larger preceding R stimuli (3.9 pV) than I stimuli (0.6 pV) in the predictable runs, the difference between the two being significant (p ~0.05). A similar comparison based on 4 set traces cannot, of course, be made for the unpredictable runs due to the random order of the tones. In light of what has been said in the literature (e.g. Tueting and Sutton, 1973) concerning the significance of the P3 or P300 component, a search was made for convincing evidence of a discrete wave at this point in our records. None was revealed. In the 4 set traces (fig. 1), however, there were signs of a much slower positive wave in the EEG extending from about 200-500 msec post-stimulus. Therefore, as well as taking the conventional measure of P300, namely positivity at a latency 300 msec relative to that at the stimulus onset, the same measure was taken at latency 400 and 500 msec. In the 4 set records of the predictable runs R minus I differences were positive in all seven subjects for the P300 measure (p
and partial correlations
between
CNV, Nl-P2,
172
R. T. Wilkinson and S. M. Ashby
fable 1. Product-moment correlations and partial correlations between CNV, P300, 400, 500 and Nl-P2. Correlations significant at p co.05 are indicated by an asterisk, p co.01 by a double asterisk. Correlation Terms correlated
Absolute scores predictable condition Relevant stimuli
CNV vs. P3OO CNV vs. P400 CNV vs. PSOO Nl-P2 vs. CNV Nl-P2 vs. P300 CNV vs. P300 (Nl-P2 constant) N1-P2 vs. CNV (P300 constant) Nl-P2 vs. P300 (CNV constant)
Relevantirrelevant score
Irrelevant stimuli
-i-0.78*
+0.35
+0.70 -to.43 +0.74 +-OS7 -0.26
-0.06 -0.09 +0.35 -0.03 -0.07
+0.89** +0.80* +0.85** +0.90** +0.79* +0.67 +0.67 -0.05
and P300 (and in some cases P400 and P500) are shown in table 1. All measures were taken from the 4 set traces of the predictable condition and are in terms of either absolute level or selective attention effect (relevant minus irrelevant amplitude). The correlation between CNV and P300 was high for relevant tones but substantially less for irrelevant stimuli. Holding N l-P2 constant produced almost no change in these correlations. Correlations between Nl-N2 and the other two measures, CNV and P300, were lower and holding each of these constant substantially reduced the partial correlation of Nl-P2 with the other. In terms of selective attention effect (relevant minus irrelevant amplitude) the correlations between all three pairings of CNV, Nl-P2 and P300 were high and only seriously reduced when CNV was held constant. Finally it seemed to make little difference to the correlation levels whether the positive-going wave ‘P300’ was measured at latency 300,400 (P400), or 500 msec (P500).
4. Discussion A consensus of EP studies of selective attention suggests that the peak-to-peak amplitude of the EP from a negative deflection (Nl) at about I10 msec to a positive deflection (P2) at about 170 msec is larger following relevant, as compared with irrelevant, stimuli in behavioural situations calling for the exercise of selective attention, but only when that situation is predictable in that the subject knows roughly when a relevant or irrelevant stimulus will occur (Chapman and Bragdon, 1964; Davis, 1964; Spong, Haider and Lindsley, 1965 ; Debecker and Desmedt, 1966; Rietveld, Tordoir and Hagenouw, 1966; Naatanen, 1967 (Exp. III); Shea& and Chapman, 1969). Where relevant and irrelevant stimuli occur in random order and at random intervals of not less than 1 set it is found, with but one exception (Eason,
Attention,
CN V, and evoked potential
173
Harter and White, 1969), that Nl-P2 is the same for both relevant and irrelevant stimuli (Donchin and Cohen, 1967; NaiBtanen, 1967 (Exp. II); Smith, Donchin, Cohen and Starr, 1970; Hartley, 1970; Karlin, Martz and Mordkoff, 1970). Since in practice we appear as capable of attending to random stimuli as to alternating stimuli these latter results have discouraged the view that the amplitude of the main N-P2 wave of the EP can indicate in any general way that selective attention is being paid to the stimulus concerned. However, in none of the experiments cited above has it been possible to make direct comparison between alternating and random modes of presentation. Usually these contrasting forms of the test have appeared in different experiments with other factors varying as well. One purpose of the present study was to make such a direct comparison by giving predictable and unpredictable forms of the test to the same subjects. The outcome has been that previous findings have been confirmed. The EP was larger for relevant stimuli than for irrelevant stimuli with alternating presentation but not with random order presentation. Comparisions within subjects were able to reveal that the absence of a relevant/irrelevant difference with unpredictable presentation was because both stimuli produced EPs of high amplitude equal to that of the relevant stimuli in the predictable alternating setting. This suggests a solution to the problem of why the effect fails to appear when relevant and irrelevant stimuli occur unpredictably: both stimuli are effectively relevant as far as the EP is concerned merely because the onset of either one presents task-relevant information. With alternating presentation no task-relevant information is passed when a predictably irrelevant stimulus occurs at a predictable point in time. It was to solve the problem of the absence of relevant/irrelevant difference with unpredictable presentation that Naatanen (1967, 1970) used longer time constant recordings which permitted CNVs to appear in the records of his condition in which relevant and irrelevant stimuli alternated. He found, as we have, that CNVs were present before relevant but not before irrelevant stimuli. We have also shown that the relevant/irrelevant difference in the EP amplitude correlated across subjects with the degree to which the CNV at the point of relevant stimulus onset exceeded that at the point of irrelevant stimulus onset. Paradoxically, this aspect of our results provides support for Naatanen’s (1967) suggestion that the EP, far from reflecting stimulus relevance, is a function merely of the amplitude of the CNV upon which the stimulus impinges, the CNV itself reflecting the level of cortical activation. The question remains then, does the main Nl-P2 component of the auditory EP reflect selective attention, or if not why does it appear to do so in many experiments ? Before examining the question further it may be helpful to consider the
174
R. T. Wilkinson
and S. M. A&b?’
behaviour of the late positive wave which we call, for convenience, but without prejudice, P300. It is difficult to know whether this is the same corn. ponent that has been referred to as the ‘late positive component’ by SuttonBraren, Zubin and John (1965), ‘P3’ by Wilkinson and Morlock (1967). or ‘P300’ by Hillyard et al. (1971). In the present records it certainly was not a sharp transient wave like those waves whose amplitude Wilkinson and Morlock found to be related to reaction time. Hovvever, there are other authors whose studies have presented pictures of broad vvav’es similar to those reported here and who have referred to them as ‘P3’ or ‘P300’. Such waves have been claimed to vary in amplitude with stimulus probability or uncertainty (Sutton et al., 1965; Sutton. Tueting, Zubin and John, 1966: Tueting et al., 1971). relevance (Donchin and Smith, 1970; Sheatz and Chapman, 1969; Wilkinson and Lee, 1972). and both discriminability (Hillyard et al., 1971) and response criterion (Paul and Sutton. 1972) in auditory signal detection. It is important in this context to distinguish clearly between P300 and the main Nl-P2 component of the EP. Unlike Nl-P2, which is highly stimulus bound, a P300 wave can appear with no stimulus delivery at all if the stimulus is expected at a particular point in time (Barlow, Morrell and Morrell. 1965; Sutton et al., 1966: Klinke. Fruhstorfer and Finenzeller, 1968). This P300 has the same spatial distribution about the cortex and the same temporal relationship to the overt motor response as the P300 wave which may follow a stimulus (Picton, Hillyard and Galambos, in press). On the other hand, Wilkinson and Morlock (1967) showed that their P3 vanished completely from the post-stimulus trace when no reaction time responses were made to their stimuli, whereas the Nl-P2 wave is always present when a stimulus occurs, albeit perhaps at reduced amplitude if the stimulus intensity is low. In the present data P300, as defined here, reflected both stimulus relevance and stimulus unpredictability, but in no simple way: it was larger with relevant stimuli, but only with predictable presentation and then only significantly so in the 4 set traces. It was larger with unpredictable stimuli, but only vvhen they were irrelevant. This simplifies to the fact that, as with Nl-P?, P300 was small when stimuli were predictably irrelevant. This is in general agreement with the current view that positivity at 300 msec post-stimulus reflects the degree to which a slimulus resolves uncertainty (see Tueting and Sutton. 1973, for review). NBatanen (1967) has shown that any CNV which is present at stimulus onset may be returned to baseline if the stimulus is a relevant one as compared with an irrelevant one. The effect has been confirmed by Wilkinson and Lee (1972). In all of these experiments the nature of the relevant stimulus was such as to resolve uncertainty, usually related to signal detection, in a way which the irrelevant stimulus could not. This, coupled with the claim that the amplitude of P300 waves also reflects stimulus uncertainty. suggests that
Artenrion,
CN V, and evoked potential
175
there is an association between the two processes, CNV and P300. The most parsimonious suggestion is that they constitute the same process. In other words, P300 is the return of CNV to baseline (Donchin and Cohen, 1967; Donchin and Smith, 1970) and is only positive in relation to the negative level (CNV) of the EEG at the point of stimulus onset. It is a positive-going return to zero which may overshoot baseline and be peaked in a manner resembling a transient component when recordings are made with relatively short time constants. Another version of the association is that the CNV return modulates the amplitude of an existing P300 wave produced directly by the stimulus (Karlin, 1970). A third version is that changes in P300 are due to a heightened level of cortical activation of which CNV is just another sign (Naatanen, 1967, 1969). Various authors have attempted to assess the validity of these suggestions by relating the level of CNV at stimulus onset to the amplitude of P300 (Lombroso, 1970; Donchin and Smith, 1970; Small and Small, 1970; Donchin, Gerbrandt, Leiffer and Tucker, 1972) though none actually correlate the two. In general these studies fail to agree, some suggesting a relationship and some not. In this study the correlation between absolute level of CNV and P300 was relatively high for relevant stimuli (+0.78) but much lower for irrelevant ones (+0.35). This again suggests that the relationship depends not just upon the pre-stimulus level of CNV but also upon whether the stimulus is more (relevant) or less (irrelevant) likely to cause CNV to return to baseline. In many of the earlier studies which examined the CNV/P300 association there were differences between stimuli either within or between conditions which would be expected to influence their relevance and consequently, on the present hypothesis, their ability to return any CNV that was present to baseline. To the extent that the latter may influence positivity at 300 msec we would not necessarily expect prior CNV level alone to correlate with P300 except under conditions where stimulus relevance is kept reasonably constant or the parameter is the difference between relevant and irrelevant stimuli. Where these conditions have been met in the present study the correlations between prior CNV and P300 have been substantial and significant. Furthermore these correlations were maintained when the positive-going wave was sampled at 400 and 500 msec latency. This shows that the effects observed cannot have been due to the variation of some late component of the EP itself at around 300 msec latency due either to its summation with the CNV resolution (Karlin, 1970) or to that component being augmented in some way by the heightened cortical excitation which Naatanen (1967, 1970) suggests is the concomitant of CNV. Thus the present data support, and previous data do not effectively discount, the view that the kind of slow positive or P300 waves we have recorded constitute the reactive return of CNV to baseline as reproduced by the typical finite time constant recording system. The same may be true for
176
R. T. Wilkinson
and S. M. Ashby
some of the longer and less transient P300 waves reported elsewhere and even shallower ones when time constants are short. Given then, that a CNV is present in the first place, if it can be accepted that the triggering of its return and the latency of that process depends upon the relevance, uncertainty, discriminability, or motivational importance of the stimulus, many of the empirical results concerning P300 become easier to explain. This may be done either on the basis of CNV return being confused with a discrete P3 wave of the EP or, more probably, of a selectively triggered CNV resolution summating with an existing P3. Before resting this case, however, a study by Donald and Goff (1971) should be considered. These authors, aware of the possibility that both prior CNV and the ability to return CNV to baseline might contribute to the CNV/P300 relationship, attempted to control both. Following a warning stimulus their subjects received a shock which was either relevant or not relevant to the task of making a choice response to a third and final stimulus. CNV level at the onset of the second, shock stimulus was controlled by selecting traces which contained the same CNV deviation from baseline. An attempt was made to control CNV return by requiring subjects to delay an overt response to the shock stimulus until the arrival of the third choice response stimulus some 500-1500 msec later. In spite of the controls they observed variations in P300 as a function of the relevance of the shock stimulus, and thus they claimed to have proved a dissociation between CNV and P300. However, praiseworthy as this attempt is, it is not wholly convincing. CNV can develop as soon as 200400 msec following a warning stimulus (Posner and Wilkinson, 1969; Rebert and Knott, 1970) if the interstimulus interval between warning and imperative stimulus is reasonably short. It seems quite possible that the CNV before the second, shock stimulus may in fact have returned towards baseline and then redeveloped rapidly in preparation for the third stimulus to which a response had to be made, as found by Wilkinson and Spence (1973). Unfortunately, the rather large EPs to the shock make it difficult to be sure of this from examination of the traces shown by Donald and Goff. Replication using a weak stimulus at this point would be desirable, but meanwhile it seems doubtful whether this study provides sufficient evidence to reject the view that CNV and P300 are associated, or indeed that the slow positive-going wave observed in the present study and in a number of others constitutes the return of CNV to baseline and is not a potential evoked directly by the stimulus, as Nl-P2 seems to be. We return now to our main concern, a decision as to whether Nl-P2 does or does not reflect selective attention. Although there have been suggestions that the return of CNV to baseline may summate with a discrete P3 wave in the EP (Karlin, 1970), the earlier Nl-P2 wave has been neglected in this respect, except for the early work of Naatanen (1967), presumably because it was thought that the CNV could not return quickly enough to summate
Attention, CN V, and evoked potential
177
of the EP. An inspection of the traces in fig. 1 strongly suggests that it can. These phenomena support the proposition made by Wilkinson and Lee (1972) that Nl-P2 appears to reflect selective attention because it summates with the CNV return following selectively upon relevant stimuli. These authors argued that the positive-going CNV return was the true feature of the post-stimulus trace to reflect selective attention because its amplitude was related to selective attention performance, whereas that of Nl-P2 was not. It was unfortunate that Wilkinson and Lee were unable to average the pre-stimulus EEG and thus observe the presence of prior CNV rather than infer it. In the present study the omission was rectified. In fig. 1, CNVs can be seen preceding the relevant stimulus, returning to baseline with its onset, and summating with the Nl-P2 wave in such a way as to make it appear amplified following relevant, as compared with irrelevant, stimuli. Other traces can be found in the CNV literature showing the same effect, for example during the vigilance task used by Wilkinson and Haines (1970, see fig. la, especially subject 2). If earlier arguments can be accepted that the present late positive wave (P300-500) represents the extent of CNV return to baseline, the Wilkinson and Lee proposal is supported empirically by the high correlations between pre-stimulus CNV, P300, 400, 500 and Nl-P2 in the degree to which they reflected relevant/irrelevant differences. To summarise, therefore, it is suggested that two factors, (1) stimulus onset CNV level, and (2) ability of the stimulus to return CNV to baseline, decide the amplitude of ‘Nl-P2’ as a function of selective attention. To derive further support for this general proposition we may consider the correlations and partial correlations between the present CNV, P300 and Nl-P2 in terms of absolute levels and amplitudes for stimuli in the predictable condition (table 1). For both relevant and irrelevant stimuli the correlation between CNV and P300 remained virtually unchanged when Nl-P2 was held constant, indicating that Nl-P2 was not influencing these two measures. On the other hand, holding either CNV or P300 constant reduced the correlation of Nl-P2 with the other, suggesting again that CNV at stimulus onset and the degree of CNV resolution by the stimulus (as indicated by the present P300 measure) are the true determinants of the amplitude of Nl-P2 as selective attention is varied.
with this component
References Barlow, J. S., Morrell, L. and Morrell, F. (1965). On evoked responses
in relation to temporal conditioning to paired stimuli in man. MIT. Research Laboratories Electronic Quarterly Progress Report, 78, 263-272. Chapman, R. M. and Bragdon, H. R. (1964). Evoked response to numerical and nonnumerical stimuli while problem solving. Nature (London), 203, 1155-1157. Davis, H. (1964). Enhancement of evoked cortical potentials in humans related to tasks requiring a decision. Science, 145, 182-183. Debecker, J. and Desmedt, J. E. (1966). Rate of intermodality switching disclosed by
R. T. Wilkinson and S. M. Ashby
178
sensory evoked potentials averaged during signal detection tasks. Journal of Phy.siology (London), 185, 52-53. Donald, M. W. and Gaff, W. R. (1971). Attention-related increases in cortical responsivity, dissociated from the contingent negative variation. Science, 172, 1163-1166. Donchin, E. and Cohen, L. (1967). Averaged evoked potentials and intra-modality selective attention. Electroencephalography and Clinical Neurophysiology, 22, 537-546. Donchin, E., Gerbrandt, L. A., Leiffer, L. and Tucker, L. (1972). Is the contingent negative variation a motor response? Psychophysiology, 9, 178-l 79. Donchin, E. and Smith, D. B. D. (1970). The contingent negative variation and the late positive wave of the average evoked potential. Electroencephalography and Clinical Neurophysiology,
29, 201-203.
Eason, R. G., Harter, M. R. and White, C. T. (1969). Effects of attention and arousal on visually evoked cortical potentials and reaction time in man. Physiological Behaviour,
4, 283-289.
Gilden, L., Vaughan, H. G. and Costa, L. D. (1966). Summated human EEG potentials with voluntary movement. Electroencephalography arrd Clinical Neurophysiology, 20, 433-438.
Hartley, L. R. (1970). The effect of stimulus relevance on the cortical evoked potentials. Quarterly Journal of Experimental
Hillyard,
S. A. and Galambos,
encephalography
Psychology,
22, 531-546.
R. (1970). Eye movement
and Clinical Neurophysiology,
artefact in the CNV. Electro-
28, 173- 182.
Hillyard, S. A., Squires, K. C., Bauer, J. W. and Lindsay, P. H. (1971). Evoked potential correlates of auditory signal detection. Science, 172, 1357-1360. Karlin, L. (1970). Cognition, preparation and sensory evoked potentials. Psychological Bulletin, 73, 122-136.
Karlin, L., Martz, M. J. and Mordkoff, A. M. (1970). Motor performance and sensory evoked potentials. Electroencephalography and Clinical Neurophysiology,, 28, 307-3 13. Klinke, R., Fruhstorfer, H. and Finenzeller, P. (1968). Evoked responses as a function of external and stored information. Electroencephalowaphv and Clinical Neurophysiology,
25, 119-I 22.
Lombroso, C. T. (1970). The CNV during tasks requiring choice. In: Evans, C. R. and Mulholland. T. B. (Eds.) Attention in Neurophysiology. Butterworth: London. 64-69. Naatanen, R. (1967). Selective attention and evoked potentials. Anna/es Academiae Scientiarum
Naatanen,
Fennicae,
25, l-226.
R. (1969). Anticipation
of relevant stimuli and evoked potentials.
Perceptual
and Motor Skills, 28, 639-646.
Naatanen. R. (1970). Evoked potential. EEG and slow potential correlates of selective attention. In: Sanders, A. F. (Ed.) Attention and Performance III, Acta Psychologica. North-Holland: Amsterdam, 178-192. Paul, D. D. and Sutton, S. (1972). Evoked potential correlates of response criterion in auditory signal detection. Science, 177, 362-364. Picton, T. W., Hillyard, S. A. and Galambos, R. (In press). Cortical evoked responses to omitted stimuli. In: Livanov, M. N. (Ed.) MajorProblemsofBrain Electrophysiology. U.S.S.R. Academy of Sciences. Posner, M. I. and Wilkinson, R. T. (1969). On theprocess ofpreparation. Paper presented to Psychonomic Society (USA), Nov. 1969. Rebert, C. S. and Knott, J. R. (1970). The vertex non-specific potential and latency of contingent negative variation. Electroencephalography and Clinical Neurophysiology, 28, 561-565.
Reitveld, W. J., Tordoir, W. E. M. and Hagenouw, J. R. B. (1966). Influence of attentiveness, of vigilance task difficulty and of habituation on cortical evoked responses and on artefacts. Acta Physiologica et Pharmacologica Neerlandica, 14, 18-37. Sheatz, G. C. and Chapman, R. M. (1969). Task relevance and auditory evoked responses. Electroencephalography
and Clinical Neurophysiology,
26, 468-475.
Siegel, S. (1956). Nonparametric Statistics. McGraw-Hill: New York. Small, J. G. and Small, I. F. (1970). Interrelationships of evoked and slow potential responses. Diseases of the Nervous System, 31, 459-464.
Attention,
CN V, and evoked potential
179
Smith, D. B. D., Donchin, E., Cohen, L. and Starr, A. (1970). Auditory averaged evoked potentials in man during selective binaural listening. EIectroencephalographv and Clinical Neurophysiology,
28, 146-152.
Spong, P., Haider, M. and Lindsley, D. B. (1965). Selective attentiveness and cortical evoked response to visual and auditory stimuli. Science, 148, 395-397. Sutton, S., Braren, M., &bin, J. and John, E. R. (1965). Evoked potential correlates of stimulus uncertainty. Science, 150,1187-l 188. Sutton, S., Tueting, P., Zubin, J. and John, E. R. (1966). Information delivery and the sensory evoked potential. Science, 155, 1436-1439. Tueting, P. and Sutton, S. (1973). In: Kornblum, S. (Ed.) Attention and Performance. Academic Press: New York. Tueting. P.. Sutton. S. and Zubin, J. (1971). Quantitative evoked potential correlates of the probability of events. Psychophysio;ogyt 7, 385-394. _ Wilkinson, R. T. and Haines, E. (1970). Evoked response correlates of expectancy during vigilance. Acta Psychologica, 33, 402-413. Wilkinson, R. T. and Lee, M. V. (1972). Auditory evoked potentials and selective attention. Electroencephalography and Clinical Neurophysiology, 33, 41 l-41 8. Wilkinson, R. T. and Morlock, H. C. (1967). Auditory evoked response and reaction time. Eiectroencephalography and Clinical Neurophysiology, 23, 50-56. Wilkinson, R. T. and Spence, M. T. (1973). Determinants of the post-stimulus resolution of contingent negative variation (CNV). Electroencephalography and Clinical Neurophysiology,
35, 503-509.