Intracerebral events in humans related to real and imaginary stimuli

Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands

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I N T R A C E R E B R A L EVENTS I N H U M A N S R E L A T E D TO R E A L A N D I M A G I N A R Y S T I M U L I 1 H. WEINBERG 2, W . GREY WALTER AND H. J. CROW

Burden Neurological Institute, Bristol (Great Britain) (Accepted for publication: November 14, 1969)

Several authors, e.g., Spong et al. (1965), Haider et al. (1964), Riggs and Whittle (1967) and Klinke et al. (1968) have reported observations which suggest that when an expected stimulus does not occur a cerebral event appears at a latency similar to that of potentials evoked by the stimulus. Related to those observations are reports of cerebral potentials evoked by afterimages, e.g., Garcia-Austt et al. (1964). The implication of such observations is that the brain is spontaneously reproducing those processes originally elicited or evoked by stimuli.It is as if processes were generated corresponding to the memory of past stimuli, to what may more generally be referred to as "imaginary stimuli". One of the clearest examples of cerebral events corresponding to expected but absent stimuli occurs in the results reported by Klinke et aL (1968). They presented click stimuli in triplets with 1 sec intervals between stimuli within triplets. Occasionally they omitted the second stimulus within a triplet and observed a negative deflection at a latency approximating that for the second stimulus when it did occur. Because of the paradigm which Klinke used the deflections observed could be related to the contingent negative variation (CNV) since negative expectancy waves occur when stimuli follow each other in such a way that the first establishes a clear expectancy of the second. A major difficulty encountered in investigaa This study was supported in part by grants from the Medical Research Council and National Research Council of Canada, and by the W. Clement and Jessie V. Stone Foundation of Chicago. 2 Present address: Department of Psychology, Simon Fraser University, Burnaby 2, Vancouver, B.C., Canada.

tions of cerebral potentials related to expected but absent stimuli is the inaccuracy of the subject's estimation of when the expected stimuli should occur. The use of a stimulus index (e.g., a stimulus in another modality) which occurred simultaneously with the expected stimulus would be a contributing factor in any cerebral event observed when expected stimuli either occurred or were absent. Attempts to subtract that part of an evoked potential attributable to the stimulus index (which is itself a stimulus) and retain that portion attributable to expectancy presents many methodological and theoretical problems. When a stimulus preceding the expected stimulus is used as an index of when stimuli are expected to occur (e.g., Klinke et al. 1968) inaccuracies in time estimation must result and introduce variability in latencies (with respect to the index) of processes which are related to expected but absent stimuli. Such variability in latency of processes corresponding to imaginary stimuli would necessarily reduce the degree of resolution possible with averaging techniques since averaging must be time-locked to a predetermined signal. In our experiments we were specifically ininterested in whether cerebral events resembling evoked potentials would occur in the absence of expected stimuli. We allowed subjects to establish their own expectancies without the use of predetermined probabilities of stimulus occurrence and designed a procedure which would minimize the loss of resolution due to inaccuracies of time estimation. METHOD

The five subjects we used were undergoing Electroenceph. clin. Neurophysiol., 1970, 29:1-9

2

H. WEINBERG

for severe intractable anxiety and obsessive disorders as in-patients at the Burden Neurological Institute. The clinical treatment, developed by Crow et al. (1961), makes use of indwelling gold electrodes chronically implanted for periods of up to 6 months. The electrodes from which we recorded were not used for making electrolytic lesions (a technique in the treatment procedure) since they were located in or near gray matter; they were in orbito-frontal and cingulate cortex and on the surface of the superior frontal cortex. All patients volunteered for the experiment and were fully cooperative during the procedure. At the time of the experiment they were either drug-free or on very small doses. They were informed that the purpose of the experiment was to measure brain function during guessing behaviour and that the procedure was not part of their therapy programme; they seemed to enjoy the experience as a game with the experimenter. We used a Beckman-Offner Type TC EEG to amplify cerebral potentials and write out ongoing activity, a PI/6100 8-channel tape recorder to store the complete data and a LLNC 8 computer for on-line averaging. All subjects lay supine in a comfortable position with eyes closed during the procedure. A small springloaded lever which could be pressed to the left or right (with respect to the subject’s position) was situated near the subject’s left hand. Before beginning the experiment all subjects were told that they could use the lever to signal whether they expected the occurrence of a stimulus. In some experiments the stimulus was the sound of a click, in others it was a flash or a mild electric shock to a finger of the right hand. The subjects were told to press the lever to the right if they expected or guessed that a stimulus would occur; to press it to the left if they did not. They were offered a reward of sixpence for every three successive correct guesses whether these were a~rmative or negative. They were advised to press the lever one way or the other at intervals of not less than about 10 set and were allowed to practise this for a few trials. Movement of the lever in either direction started the computer average; whether a stimulus was to be provided was determined on each

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occasion by the experimenter operating a switchboard according to a programme of random variations. Thus, neither the experimenter nor the subject could telf whether a guess would be right or wrong. Whenever a stimulus did occur, by the coincidence of the experimenter’s switching schedule and the subject’s lever movement. the moment of occurrence was at the instant of lever movement. The subjects therefore discovered at once whether their guess was right or wrong on every occasion. Since they worked at their own rate, within the limit specified, there was no fixed interval between guesses. Subsequent discussions with the subjects revealed considerable variation in attitude. A correct afTirmative guess seemed more satisfying than a correct

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Evoked and emitted potentials to flash stimuli. “Expect” refers to expectation of flash occurrence, numbers refer to electrodes. Bottom line shows the response evoked by randomly presented stimuli (see text). Note the shortened latency of evoked and emitted potentials in the experimental conditions. Note also the similarity of the potentials emitted in the absence of stimuli (middle, left) to those evoked by stimuli (top line). Each trace is an average of 8 trials; 8 averages are superimposed in the expectation traces and 4 in the random sets. Electroeneeph.

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negative one a l t h o u g h the chances a n d r e w a r d were the same in b o t h cases. M o s t subjects w o n several shillings (that is, there were several runs o f 3 correct guesses). This a r r a n g e m e n t p r o v i d e d f o u r c o n d i t i o n s u n d e r which cerebral activity c o u l d be s e p a r a t e l y a v e r a g e d : e x p e c t a t i o n a n d occurrence o f the

Fig. 2 Left: Two averages of evoked and emitted potentials to clicks in the right orbital cortex. Right: Superimposition of two replications of each condition from 4 left frontal electrodes in another subject. Random activity is superimposition and replication of averages from 4 electrodes simultaneously. Note similarity of responses to random stimuli and differences in responses to expected stimuli. stimulus; e x p e c t a t i o n a n d n o n - o c c u r r e n c e o f the stimulus; n o n - e x p e c t a t i o n b u t occurrence o f the stimulus; n o n - e x p e c t a t i o n a n d n o n - o c c u r r e n c e o f the stimulus. By utilizing the delay between r e c o r d a n d r e a d - o u t times o f the a n a l o g u e t a p e system we were also able to average activity d u r i n g the 1.4 sec preceding switch closure. Electroenceph. clin. Neurophysiol., 1970, 29: 1-9

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In the following account the term "evoked potential" is used for cerebral potentials recorded after occurrence of a stimulus. "Emitted potential" is used for potentials occurring when no stimulus had been presented. The term " r a n d o m stimuli" is used for control stimuli presented at the end of the experimental paradigm described above. Responses to random stimuli were recorded after the subjects had been told the experiment was over and the hand lever had been removed. " R a n d o m activity" is used to refer to spontaneous activity aperiodically averaged after responses to random stimuli had been averaged.

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The experimental procedure yielded four primary observations. The first, and most important, was the appearance of emitted cerebral potentials when stimuli were expected but did not occur; the form of the potentials resembled those evoked by stimuli. Fig. 1-4 show averaged records with visual, auditory and tactile stimuli. These indicate the degree of resemblance according to modality and demonstrate that stimulusrelated emitted activity occurred in both orbital and superior frontal regions. Similar effects have been seen also in cingulate regions. The correlation functions and coefficients in Fig. 6 and 7 provide a measure of the over-all similarity of patterns. Differences observed in responses evoked by stimuli in different modalities were reflected by differences in emitted potentials. Both evoked and emitted potentials appeared bilaterally, in homologous areas of the cortex when tactile stimuli were presented unilaterally (Fig. 4). A second effect which occurred in three of the five subjects was a shortening of latency by about 25 msec of both evoked and emitted potentials after expectation, when compared with those evoked by random stimuli (Fig. 1, 2). Fig. 3 illustrates a related phenomenon which was occasionally observed; a latency of emitted potentials which was shorter than that of both evoked potentials after expectancy and those evoked by random stimuli. A third observation of interest was a large positive shift, peaking at about 300 msec after switch closure, which appeared during the ex-

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Fig. 3 Evoked and emitted potentials to click stimuli. Note the absence of a prominent 300 msec positive deflection in

the expectancy conditions. Control recordings are of frontal electrodes Nos. 27, 28, 29, 30 and 78. Each trace is an average of 8 trials over 500 msec.

pectancy conditions and which was minimal when no stimulus occurred after subjects had indicated no expectancy. This is illustrated in Fig. 1-3, 5 and 7 and corresponds to the P3 wave described by Sutton e t al. (1967) and others. The fourth observation was a CNV (Walter e t al. 1964) preceding evoked and emitted responses in the expectancy conditions. The short time constant of the gold electrodes attenuated slow potential changes but the activity in Fig. 4, recorded with a 1 sec time constant of the amplifier, shows the presence of a slow negative Electroenceph. clin. Neurophysiol., 1970, 29: I -9

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shift in the frontal cortex, preceding both evoked and emitted responses. Control recordings of activity which followed right and left lever depression, after subjects had been informed that guessing contingencies were no longer in effect (Fig. 3-5, 7) made it clear that the above effects were not confounded by motor components associated with manipulation of the lever. Fig. 5 also demonstrates that there was no systematic activity preceding lever depression when guessing contingencies were no longer in effect. Cross-correlations and auto-correlations were used to examine relationships between some of the above observations. The programme used to

derive the correlation (or co-variance) functions normalizes the original data functions so that differences in amplitude are minimized and resemblances of wave form clarified. Thus the coefficient of 0.75 in Fig. 6 relating the pattern of "expect but no" to "expect and yes" indicates a highly significant resemblance. In this case the coefficient for "no expect but yes" was actually slightly smaller at 0.7 but that for "no expect and no", 0.3, was smallest at zero time displacement. In general, potentials emitted when stimuli were expected but did not occur correlated highly with evoked potentials of stimuli which were expected and occurred. Similarly, there were high correlations between evoked Electroenceph. c/in. Neurophysiol., 1970, 29:1 9

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function correlated best (approximately 0.8) with potentials which were evoked, approximately 0.5 with potentials emitted after expectancy and least well with potentials emitted after no expectancy (approximately 0.1). DISCUSSION

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potentials under conditions of expectancy and no expectancy. Lowest correlations were between evoked potentials under conditions of expectancy and emitted potentials under conditions of no expectancy. Comparisons of potentials evoked by random clicks with potentials evoked tinder conditions of both expectancy and no expectancy showed high correlations. Correlations computed between emitted potentials and potentials evoked by random stimuli were low; Fig. 6 presents a summary of these effects. The cross-correlations between responses to random clicks and those in conditions of expectancy show the degree of latency difference by displacement of the peak of the correlation function. An attempt was also made to synthesize a wave form which was characteristic of that which dominated evoked and emitted cerebral potentials. Fig. 7 shows the wave form which was estimated from the data in Fig. 1 and applied to the data collected from another subject. The

These results demonstrate the presence of a cerebral event which is emitted when an external stimulus is expected but does not occur. Of particular interest is the similarity of these events to potentials evoked by stimuli, which suggests that emitted potentials may reflect memory processes corresponding to the stimulus. In this experiment we were not interested in manipulating probabilities. However, although we instructed subjects to dichotomize their expectancy it must certainly be true that their subjective attitude was related to their estimation of the probability of occurrence after each decision. When subjects selected one of the two alternative actions the relative degree of certainty was presumably greater with respect to the expectancy indicated. Such an interpretation is supported by the observation that emitted potentials were absent or much smaller when subjects indicated no expectancy. We suggest that the degree to which emitted potentials occur reflects the degree of subjective probability with respect to stimulus occurrence. These effects are unlikely to be due to differential arousal. Since the subject's guess could be confirmed, and be correct under conditions of both stimulus expectancy and non-expectancy, there is no reason to believe the subject to have been more aroused when expecting than when not expecting the stimulus. The correctness of each guess contributed to the chance of a reward whether the guess was occurrence or nonoccurrence. Furthermore, such arousal differences, if they were present, would be expected to have equally differential effects when the stimulus actually occurred. Since this was not apparent it appears safe to rule out the effect of selective arousal as an important contributing factor in the results observed. Nevertheless, the reduced latency of the first components of emitted and evoked potentials during expectancy suggests a significant increase in cortical excitability, a fall in threshold or a Electroenceph. olin. Neurophysiol., 1970, 29:1 9

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Fig. 6 Auto-correlation and cross-correlation of emitted and evoked potentials. Left side: evoked potential to expected stimulus is used as the template (first trace) against which correlations of other conditions are computed. Auto-correlation in lower left shows comparisons of auto-correlation functions for expectancy and control conditions. "Yes" and "No" refer to stimulus occurrence. R :- -- Expect, Yes; R -- Expect, No; ]L + -- No expect, Yes; ]L -- No expect, No. Right side: top trace is auto-correlation of random clicks. Cross-correlations use evoked potential to random clicks as template against which other conditions are correlated. The term random click above the first cross-correlation identifies the template, lettering along the side identifies the condition. Scale of correlations: Abscissa -- 250 msec, ordinate intervals are correlation coefficients (1.0 at top). Epoch of averaged evoked response is 500 msec; each trace is an average of 8 sweeps.

shortened pathway. The last possibility is plausible in the case of the emitted potentials since there is no reason to suppose activity in an afferent tract when there is n o external stimulus. Since the expected evoked responses also had a shorter latency, it may be that in these c o n d i t i o n s expectancy of a specific stimulus is associated with a m o d u l a t i o n of cortical excitability with a c o n t o u r resembling that of the expected response b u t preceding it by a b o u t 25 msec. It will be noticed that in records such as those in Fig. 1 a n d 2 the trace starts above the baseline. The averaging p r o g r a m m e normalizes the voltage for a b o u t 1 sec before the average, that is, it sets the starting level to zero whatever the actual baseline level. This m e a n s that the

true potential at the start of the trace on switch closure was even higher t h a n indicated. This is shown clearly in Fig. 4 which includes a period of 1.4 sec before closure. This negative wave is a c o m b i n a t i o n of the Bereitschaftpotential or I n t e n t i o n Wave that precedes a v o l u n t a r y movem e n t a n d a C N V associated with expectancy. Evidence for increased cortical excitability at the peak o f the C N V has been reported by M c A d a m (1968) a n d a lowered threshold to direct electrical s t i m u l a t i o n of the cortex at this phase has been observed by one of us (Walter, work in progress). A t t e m p t s to find systematic p a t t e r n i n g of rhythmic activity preceding responses which were associated with either expectancy or with differential a n t i c i p a t i o n of right a n d left switch closure Electroenceph. clin. Neurophysiol., 1970, 29:I-9

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have been unsuccessful. Averages of response duration (Fig. 5) have shown that evoked and emitted potentials were generally complete before the switch was released. This observation and the fact that switch closure and release did not lead to systematic emitted potentials prior to or after the response suggest that electrical activity related to differential anticipation of the alternative motor behaviour was not confounding the potentials observed after stimulus expectation. From what we know about the nervous system there is no reason to assume that the experience of an image depends on the establishment of those processes originally involved in the registration and coding of the stimulus. However, an interesting implication of our observations is that an assumption of this nature might be a reasonable working hypothesis. The fact that emitted potentials correlate well with potentials which are evoked by stimuli suggests that the underlying electrophysiological processes which

Recordings were made from gold intracerebral electrodes in orbital and cingulate cortex and subdural electrodes on superior frontal cortex in five patients under treatment for chronic obsessional and anxiety disorders. The subjects were instructed to guess whether or not they would receive a stimulus in the form of a flash, click or electric shock to the finger. They were told to move a lever to the right when they expected a stimulus and to the left when they did not. A reward was offered for every three successive correct guesses. Movement of the lever in either direction started a L I N C 8 averaging and provided a stimulus or not according to a switching programme operated by the experimenter. Sets of averages of eight trials each were collected in the four conditions: expectation-occurrence, expectation-non-occurrence, no expectation-occurrence, no expectation-non-occurrence. Averages were also taken of responses to random stimuli and of intrinsic activity when the lever was moved without guessing or stimuli. Clear cerebral events, termed "emitted potentials", were observed when stimuli were expected but did not occur. The emitted potentials resembled those evoked when real stimuli were presented on switch closure, suggesting that they may reflect memory processes corresponding to the perception of real events. In some experiments the latency of the emitted potentials was significantly shorter than that of responses evoked by real random stimuli, suggesting a rise in cortical excitability with expectancy. A positive deflection peaking at about 300 msec often appeared following switch closure, particularly with expectancy, and a negative variation usually preceded and accompanied this action. R~SUM~ EVI~NEMENTS INTRACI~REBRAUX CHEZ L'HOMME EN LIAISON AVEC DES STIMULI RI~ELS ET IMAGINAIRES

Des enregistrements ont 6t6 pratiqu6s au moyen d'61ectrodes d'or intrac6r6brales situ6es Electroenceph. clin. Neurophysio[., 1970, 29:1 9

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REAL AND IMAGINARY STIMULI

dans le cortex orbitaire et cingulaire et d'61ectrodes sousdurales situ6es sur le cortex frontal sup6rieur chez cinq malades trait6s pour troubles obsessionnels et anxieux chroniques. Les sujets reqoivent la consigne de pr6voir s'ils vont ou non recevoir un stimulus sous forme d'un flash, d'un clic ou d'un choc 61ectrique au doigt. II leur est demand6 de bouger un levier vers la droite quand ils attendent un stimulus, vers la gauche quand ils ne l'attendent pas. Une gratification leur est offerte pour chaque succession de trois paris corrects. Le mouvement du levier dans l'une ou l'autre direction met en route un moyenneur L I N C 8 et fournit ou non un stimulus suivant le programme de commutation actionn6 par l'exp6rimentateur. Des s6ries de moyennes de huit essais chacune sont recueillies dans les quatre conditions suivantes: attentesurvenue, attente-non survenue, pas d'attentesurvenue, pas d'attente-non survenue. Les moyennes des r6ponses aux stimuli al6atoires et de l'activit6 intrins6que quand le levier est boug6 sans qu'il n'y ait de pr6vision ni de stimulus sont 6galement effectu6es. Des 6v6nements c6r6braux 6vidents, d6nomm6s "potentiels 6mis" sont observ6s quand les stimuli sont attendus mais ne surviennent pas. Ces potentiels 6mis ressemblent 5. ceux qui sont 6voqu6s quand les stimuli r6els sont pr6sent6s la fermeture du commutateur, ce qui suggbre qu'ils reflbtent des processus mn6siques correspondant ~ la perception d'6v6nements r6els. Dans certaines exp6riences, la latence des potentiels 6mis est de faqon significative plus courte que celle des r6ponses 6voqu6es par stimuli al6atoires r6els, ce qui suggbre que l'attente

augmente l'excitabilit6 corticale. Une d6ftexion positive dont le pic se situe 5. environ 300 msec apparait souvent apr6s la fermeture du commutateur, particuli6rement en cas d'attente, et une variation n6gative pr6c6de et accompagne habituellement cette action. We are deeply indebted to Dr. Ray Cooper and Mr. W. J. Warren for their assistance in the programming and operation of the computer. REFERENCES CROW, H. J., COOPER, R. and PHILLIPS, D. J. Controlled multifocal leucotomy for psychiatric illness. J. NeuroL Neurosurg. Psychiat., 1961, 24: 353-360. GARCiA-AUSTT,E., BOGACZ,J. and VANZULLI,A. Effects of attention and inattention upon visual evoked response. Electroenceph. clin. Neurophysiol., 1964, 17: 136-143. HAIDER, M., SPONG, P. and LINDSLEY, D. B. Attention, vigilance and cortical evoked potentials in humans. Science, 1964, 145: 180-182. KLINKE, R., FRUHSTORFER, H. and F1NKENZELLER, P. Evoked responses as a function of external and stored information. Electroenceph. clin. Neurophysiol., 1968, 25:119-122. MCADAM, D. W. Increases in CNS excitability during negative cortical slow potentials in man. Electroenceph. clin. Neurophysiol., 1968, 26: 216-219. RIGGS, L. A. and WHITTLE, P. Human occipital and retinal potentials evoked by subjectively faded visual stimuli. Vision Res., 1967, 7: 441-451. SPONG, P., HAIDER, M. and LINDSLEY, D. B. Selective attentiveness and cortical evoked responses to visual and auditory stimuli. Science, 1965, 148: 395-397. SUTTON, S., TUETING, P., ZU81N, J. and JOHN, E. R. Information delivery and the sensory evoked potential. Science, 1967, 155: 1436-1439. WALTER,W. G., COOPER,R., ALORIDGE,V. J., MCCALLUM, W. C. and WINTER, A. L. The contingent negative variation: an electric sign of sensori-motor association and expectancy in the human brain. Nature (Lond.), 1964, 203:380 384.

Reference: WEINBERG,H., WALTER,W. G. and CROW,H. J. Intracerebral events in humans related to real and imaginary stimuli. Electroenceph. clin. Neurophysiol., 1970, 29: 1-9.