ACTA NEUROBIOL. EXP. 1977, 37 : 311-324 AVERAGED CORTICAL EVOKED POTENTIALS TO RECOGNIZED AND NON-RECOGNIZED VERBAL STIMULI E. KOSTANDOV and Y. ARZUMANOV Serbsky Central Research Institute of Forensic Psychiatry Moscow, USSR Abstract. Averaged evoked potentials (AEPs) to visually presented neutral and emotionally significant words were recorded from the occipital area and vertex in 37 adults with normal vision. In the first experiment all the stimuli presented on the screen with time exposure 200 ms were supraliminal and were easily recognized by the subjects. In the second experiment time exposure of the stimuli was 15 ms. All the subjects were then unable to recognize the stimuli. The AEPs were observed to physically feeble but emotionally significant stimuli. Thus the analysis of semantic properties of the emotional word may take place in the cerebral cortex without its awareness. INTRODUCTION A great amount of data has been accumulated in recent years that averaged evoked potential (AEP) of the cortex, particularly its late components, reflect not so much the physical properties of the stimulus, as its biological and psychological significance for the subject (6, 11, 13, 16). This provided the ground for the use of the AEP method to study the effect of positive and negative emotions on the perception of external signals. An increase in the amplitude of late AEP waves in response to the stimuli accompanied by emotions of fear was shown in a number of experiments carried out on cats (12, 14, 18).
Despite a great interest of psychologists and neurophysiologists in the role of emotions in perception, up till now no experiments have been conducted to study cortical evoked activity elicited by emotional words. In experiments with subjects unaware of the relation between conditioned stimulus and negative emotion, Begleiter et al. (2, 3) demonstrated a decrease in AEP amplitude. In experiments where subjects were aware of this relationship, the AEP amplitude to a conditioned stimulus of negative emotion was, on the contrary, higher than in the case of a neutral stimulus or positive emotional stimulus. Shevrin et al. (23, 24) reported that in the absense of conscious discrimination, there may nevertheless be present an electrocortical discrimination related to differences in stimulus content, which are also revealed in verbal associations. We were interested in establishing relations between perception and the evoked electrical activity of the cortex. As it is known, the recognition thresholds for emotional words are quite different from the thresholds for neutral ones. Decreased as well as increased recognition thresholds were observed for emotional words, the latter accounting for approximately two-thirds of the cases (19, 21). Dixon and Lear (7) suggested that "perceptual defense" is conditioned by preaware changes of cortical activity by impulses from the reticular formation. According to our hypothesis (19). the changes of the recognition threshold for emotional words are caused by impulsation from the limbic system, the "center" of emotional behavior. Activation of the cortex to an emotional verbal stimulus may take place prior to its conscious recognition. This results in the changes of the recognition threshold. The neural mechanism seems to be important for understanding the physiological basis of preception changes of emotionally significant words, and, in particular, for understanding the increase of the recognition thresholds and, finally, the so-called subconscious emotions. This supposition required experimental verification. METHODS Investigations were conducted on 37 adult patients, 20 to 40 years of age, all with normal vision. They were in a state of emotional stress caused by jelousy. The investigations were carried out in a dark, sound-proof room with the subjects seated comfortably in a semireclined position with the eyes open. Neutral words and "conflict" words associated with the stressful situation were used as stimuli. The words, green in color, appeared on the screen placed 1.8 m from the subjects' eyes. The screen
consisted of electroluminiscent symbols 4 X 2.5 cm in size with rapid decay (1 ms). The time of exposition could be set beginning from 5 ms. The investigation started after 10 min adaptation to dark with the establishment of the recognition threshold, using, the method described by one of us (19). Further, we recorded AEP to this word from the vertex and the occipital area. The following preliminary instruction was given to the subject: "Look attentively at the screen and try to read the word but do not pronounce it, only count to yourself the number of times you could manage to do it". In the Experiment I the recognition threshold was established for two neutral words and AEPs to them were recorded. In the same session this procedure was repeated with an emotional word. In control sessions we established the perception thresholds and recorded AEP for three neutral words only. All the stimuli in this experiment were supraliminal (exposure time, 200 ms, flash intensity, 0.1 Lux $- 20 /0). In the Experiment I we examined 23 subjects; a total of 156 averaged responses to neutral words and 91 to emotional words were taken for statistics. The Experiment I1 differed from the Experiment I as to the physical parameters of t.e applied stimuli. The duration of all verbal stimuli was 15 ms; flash intensity, 0.05 lux k 20 /o. Before each test the subject was given the following instruction: "Look at the screen and try to read a word that will appear there. If you manage to read it, count how many times this word appears on the screen". After each recording of AEPs the subject was asked whether he was able to identify the word. The subjects were unable to recognize the verbal stimuli and perceived them as a dim flash of Light on the screen, although from their verbal report at the end of the experiment it could be seen that they tried to identify the word. In some cases the AEPs to the same unrecognized neutral and emotional words were recorded repeatedly (4-5 times) during different experimental days. At the end we used the same words, with the parameters of the Experiment I, which enabled the subjects to read the word. Thus we were able to compare AEP to the same words, unrecognized and recognized. In the second experiment we examined 14 subjects. The electrical activity was measured monopolarly. Active electrodes were placed on the vertex and occipital area (2.5-3 cm above the inion and 2 cm to the left of midline); the reference electrode was placed on the left ear lobe. The potentials via the amplifiers of the "Nichon Kohden" ME-132 electroencephalograph (time constant - 0.3 s) were transmitted to an ART-1000 computer. Analyzing time was 100 ms. Fifty responses to visual verbal stimuli were averaged. Time exposure of words was 200 ms. Flash intensity of all stimuli was identical
(0.1 lux f 20 /o). In each experiment we presented words with an equal number of letters. The stimuli were presented at the rate of 1 flash/5 s. After each experimental session the subject reported his impressions. The AEPs were photographed from an oscilloscope of the ART-1000. The peak latencies and the amplitudes of the negative wave N200 and the positive wave P300 were analyzed. The amplitude was measured from peak to peak. Data were analysed using Student t-test. RESULTS Experiment I. AEP to recognized verbal stimuli. To neutral words in the occipital area the P300 latency was 320 f 11.2 ms at an amplitude 10.9 k0.94 pv. At the vertex the P300 latency was 294 f 7.3 ms and the amplitude 8.7 k 0.43 uv. The amplitude of P300 at the inion for neutral Fig. 1. Averaged evoked potential of the cortex (AEP) to neutral words in subject Sh. P. in one session. A, AEP to the word "cabbage"; B, AEP to the word "drawing". Upper trace, vertex, lower trace, occipital area. Negative deflection is upward. The beginning of the trace coincides with the presentation of the stimulus. Epoch of analysis, the whole trace.
< stimuli was greater than at the vertex (P 0.001). Although latency of the component P300 at the vertex was shorter than at visual area, there was no significant difference between them. The negative wave N200 preceding P300 appeared with a latency 2 2 0 5 8 ms and an amplitude of 7.3 k0.9 pv. In different sessions subjects often showed varying parameters of the P300 even to the same word. However in a given session no significant differences, even to different neutral words, were observed (Fig. 1). This made it possible to compare cortical potentials with neutral and' emotional stimuli recorded in the same session. Most subjects showed AEPs of greater amplitude and of shorter latency to emotional verbal stimuli than to neutral (Fig. 2 and 3). The amplitude of the component P300 was 13 k0.82 yv, latency - 270 k 210.4 ms. The difference in parameters of the P300 wave between Fig. 2. Amplitude enhancement and latency shortening of P300 component to emotional stimulus in subject B.V. A, A E P to the neutral word "book", recognition threshold - 20 ms; B, AEP to the emotional word "arrest", recognition threshold 50 ms. Explanations as in Fig. 1.
neutral and emotional words was highly significant (P < 0.001 for amplitude values and P:< 0.05 for latency). Three subjects showed a lower P300 amplitude at the inion to emotional words than to neutral ones. The amplitude was 10k0.45 pv for neutral and 7.6 3~0.62 yv for emotional words, the difference being significant (P < 0.002). The latency to emotional words was shorter than to neutral. I I I I I I 200. 600 7000 rn sec Fig. 3. Amplitude enhancement and latency shortening of P300 wave to emotional stimulus in subject B.V. A, AEP to the neutral word "straircase", recognition threshold 30 ms; B, AEP to the emotional word "lover", recognition threshold 15 ms. Explanations as in Fig. 1. The averagc latency of the component P300 was 286+6 ms at the vertex to emotional words, similar to the latency to neutral stimuli. Although at the vertex the amplitude of this wave to emotional words was slightly greater than to neutral stimuli (emotional - 9.8 + 0.51 pv, neutral - 8.7 +. 0.43 pv), this was not statistically significant. Figures 2 and 3 show that component P300 recorded from the vertex to emotional and neutral stimuli was of nearly the same latency and amplitude.
Thus, emotional stimuli evoked changes of the amplitude and latency of the P300 in the occipital area. The latency was shorter and in most cases the amplitude increased. At the same time no significant differences were observed at the vertex to neutral and emotional visual stimuli. Experiment 11. AEPs to unrecognized verbal stimuli. At the occipital area the AEPs to neutral stimuli were recorded with the mean latency of the late positive component P300 304 f 3.2 ms. It could be seen, when compared with the same parameters of AEPs to recognized neutral stimuli in Experiment I, that there was no difference between them (Fig. 4). The same data were obtained with unrecognized emotional Fig. 4. P300 latency to neutral and' emotional words in Experiments I and 11. A, recognized words; B, unrecognized words. Empty bars, neutral words; hatched bars, emotional A A B words. words. The P300 latency in the occipital area was almost the same as in the case of neutral words (Fig. 4). Thus, to the unrecognized emotional verbal stimulus, we did not register a shortening of the latency of the late positive component which was observed during the exposure of the emotional word, recognized by the subject. At the vertex the late positive component P300 was recorded with an almost identical latency, irrespective of whether we presented a neutral or an emotional verbal stimulus, and whether it was recognized or unrecognized by the subject (Fig,. 4). The latency of the negative component N200 to emotional words. approximate that to neutral words. Thus, proceeding from the AEP latency we may consider that there is no cortical differentiation of the meaning of unrecognized words, as opposed to the supraliminal presentations where we establish precise latency difference between neutral and emotional words. However, an analysis of the amplitude value of the late components of the evoked potential proves that it is not so. Figure 5 shows that the P300 amplitude
at the occipital area to unrecognized emotional words was greater than that to neutral words (P,< 0.001) as was in the cases with recognized stimuli. The same Figure shows a pronounced difference in the extent of the cortical area involved in the facilitation. We observe an increase of the P300 amplitude to recognized emotional words at the occipital area only, which would justify the suggestion of a relatively local activation, related to the emotional component of the stimulus. The late positive wave of significantly greater value than to neutral words (P <0.05) was recorded from the occipital area as well as from the vertex to unrecognized verbal emotional stimuli. Fig. 5. The amplitude changes of P300 component in Experiments I and 11. Explanations as in Fig. 4. Here is an example illustrating this interesting phenomenon. Figure 6 shows that in subject B. Yu with pronounced manifestation of jealousy in response to the neutral word "staircase" was recorded a late positive wave P300. The amplitude at the occipital area equates 6.9 mv, at the vertex- 6.6 mv (Frame A); to another neutral word "grapes" in the same experiment - 9 mv and 7.1 mv correspondingly (Frame B). To the emotional word "lover" which was unrecognized by the subject, this component was significantly greater in both recordings: at the occipital area it was 12.5 mv, at the vertex-9.3 mv (Frame C). Thus, it follows that when an emotional word is not recognized by the subject, it causes a more diffused activation of the cortex than when the same stimulus is recognized. According to our data the extent of the cortical area involved in the facilitation depends upon the level -of awareness of the emotional verbal stimulus.
Another peculiarity of the evoked potentials to unrecognized emotional words is connected with the late negative component N200. This wave, recorded at the occipital area and at the vertex, as it was shown by the first series of experiments, did not change essentially during the presentation of recognized emotional verbal stimuli, as compared with the neutral ones. At the same time, when these words were not recognized by the subject, the negative N200 component to emotional Fig. 6. Enhancement of the cortical electrical response a t the vertex and at the occipital area to unrecognized emotional word. A, "staircase"; B, "grapes"; "lover". Upper trace, the vertex; lower trace, the occipital area. Upward deflections are negative. The arrow and the letter S indicate the moment of stimulati'ng. Epoch of analysis, the whole trace. c,
stimuli was of a greater amplitude at the inion as well as at the vertex (P < 0.001). The mean amplitude values of this wave to recognized and unrecognized neutral and emotional verbal stimuli are given in Fig. 6 and 7. Inion Vertex Fig. 7. Amplitude increasement of the late negative component N200 to unrecognized emotional words. Explanations as in Fig. 4- DISCUSSION The most permanent AEP component in our experiments was the late positive wave P300 with the latency near 300 ms. This slow positive wave is analysed in many investigations of the cortical AEP in human subjects to auditory or visual stimuli (16, 17, 22). The amplitude increases of the component P300 depend on the attentional level, the orienting reaction and the significance of the stimulus for the subject (2, 8, 10, 20, 22, 27). These changes of the evoked activity connected with the attentional shifts or significance of the stimulus were diffuse, i.e., they were observed not only in the sensory specific cortex, but in other cortical regions as well (15). The changes of AEP observed in our experiments could not be attributed to the attentional shift or orienting reaction to the stimulus, as subject's attention was sustained by the preliminary instruction to count the number of presented words. It may be suggested that the changes of the P300 parameters were partially caused by the dilatation of the pupil during negative emotional reactions. However, the data of Fleming (9) on cats and of John (16) on people have shown that the amplitude and wave form of late components of AEPs to visual stimuli are independent of pupil size. Thus the observed differences in latency and amplitude of AEPs probably depend on the affective meaning of the stimulus.
In our opinion, cortical activation which elicits the shortening of latency and the increase of AEP amplitude to emotional words, is caused by unspecific impulses from the limbic structures which integrate emotional reactions. The relation of the cortical evoked electrical activity to the functional state of the limbic system was proved in a number of experiments on animals. Sierra and Fuster (25) found in their experiments, using electrical stimulation of the hippocampus and amygdala, that the amplitude of late evoked potentials to visual stimuli was increased. Posterior hypothalamus stimulation of various intensity caused facilitation as well as inhibition of evoked visual cortical response (1, -5). The facilitation of the late positive evoked responses to recognized verbal emotional stimuli was observed at the occipital area, whereas at the vertex we did not establish any significant changes. We may consider that the facilitation of electrical cortical responses to recognized emotional visual stimuli takes place in the visual cortex and does not spread to the vertex. The difference in the amplitude of evoked potentials to neutral and emotional words, obtained in the Experiment 11, suggests that even if the verbal stimulus is not recognized, the analysis of its semantic content occurs at the cerebral cortex. Thus, to implement the corticofugal impulses, which according to our standpoint, give rise to facilitatory influence from the limbic system under the effect of the emotional stimulus, it is not obligatory that the word should be recognized by the subject. This effect may occur long before the word is recognized on the level of awareness. Numerous investigations, including our own, concerning the subliminal effect of emotional words on different functions of the organism, prove the possibility of perception of semantic word properties without awareness. This is also proved by psychological experiments on humans with split brain during which the subjects may perceive certain words and respond to them properly without awareness (26). Using AEP method we obtained additional proof of this phenomenon. The results of the registration of the evoked cortical potentials to unrecognized words definitely confirm the hypothesis on the neurophysiological mechanism of the so-called phenomenon of the psychological defense. According to this hypothesis, emotional stimulus before its recognition may change the activity of cortical neurons, which involves higher cortical (psychic) functions, and, in particular, the subjects' awareness level. Psychophysiological investigations much more often reveal an increase in the recognition threshold for emotional words, than a decrease when compared with neutral words (4, 19). At the same time, the facilitation of the evoked activity to unrecognized emotional words occurs in
all cases. This contradiction between perceptual and bioelectrical data might be at present explained by the fact that the ascending unspecific impulses caused by the emotional component of the word, have different effects on cortical structures. We think that the function of recognition of the verbal stimulus and bioelectrical cortical responses to it are implemented by various structures, which may change the level of their activity by ascending unspecific impulses. Notable is the difference in the cortical evoked activation to emotional verbal stimuli, which depends on whether these stimuli are recognized or unrecognized by the subjects. The recognized emotional visual stimuli induce changes in the amplitude and latency of the late positive wave (P300 component) only at the occipital area of the cortex. These changes are not observed at the vertex. If these emotional semantic stimuli are not recognized, the facilitation of the evoked electrical activity is diffuse and is observed at the vertex. Apart from that, in this case we observe an increase of the amplitude of P300 component as well as the late negative wave, the so-called N200 component. Another peculiarity characteristic of the stimulus recognition concerns the P300 latency, In response to the recognized emotional words the P300 wave at the occipital area develops with an essentially shorter latency than in the case of neutral words. In cases when these words are not recognized, we do not observe any changes in the AEP latency. This difference between recognized and unrecognized words confirms our suggestion as to the corticofugal mechanism of involvement of the limbic system in the cortical responses to emotional stimuli. It shows that the nature of the ascending "nonspecific" impulses is determined by the corticofugal influence. In recognition of the stimulus this "emotional" activation of the cortex is more local. We may consider that the excitation of the cortical structures, which provide the recognition of the verbal stimulus, to a certain extent, changes the nature of descending reg,ulating influences of the neocortex on the limbic system, and through the feedback mechanism changes the activity of the cortical neurons. REFERENCES 1. BAKLAVAJIAN, 0. 1967. Vegetative regulation of brain electrical activity (in Russian). Izdat. Nauka, Moscow. 237 p. 2. BEGLEITER, H. and PLATZ, A. 1969. Evoked potentials: modifications by classical conditioning. Science 166: 769-771. 3. BEGLEITER, H., GROSS, M. and KISSIN, B. 1967. Evoked cortical responses to affective visual stimuli. Psychophysiology 3: 336-344.
4. BEVAN, W. 1964. Subliminal stimulation: a pervasive problem for psychology. Psychol. Bull. 61: 81-99. 5. CHI, C. and FLYNN, J. 1968. The effects of hypothalamic and reticular stimulation of evoked responses in the visual system of the cat. Electroenceph. Clin. Neurophysiol. 24: 343-356. 6. COHEN, J. and WALTER, W. 1966. The interaction of responses in the brain to semantic stimuli. Psychophysiology 2: 187-196. 7. DIXON, N. and LEAR T. 1964. Incidence of theta rhythm prior to awareness of a visual stimulus. Nature 203: 167-170. 8. DONCHIN, E. and COHEN, L. 1967. Averaged evoked potentials and intramodality selective attention. Electroenceph. Clin. Neurophysiol. 22: 537-546. 9. FLEMING, D. 1969. Modified pupillary diameter and evoked potential component variation in waking cats. Electroenceph. Clin. Neurophysiol. 27: 84-86. 10. GARCIA-AUSTT, E., BOGACZ, J. and VANZULLI, A. 1964. Effects of attention and inattention upon visual evoked response. Electroenceph. Clin. Neurophysiol. 17: 136-143. 11. GASANOV, V. 1965. Investigation of thresholds of evoked potentials in the cortical projection of the conditioned stimulus (in Russian). Zh. Vyssh. Nervn. Deyat. 15: 295-302. 12. GERKEN, G. and NEFF, N. 1963. Experimental procedures affecting evoked responses recorded from auditory cortex. Electroenceph. Clin. Neurophysiol. 15: 947-957. 13. HAIDER, M., SPONG, P. and LINDSLEY, D. 1964. Attention, vigilance and cortical evoked potentials in humans. Science 145: 180-182. 14. HALL, R. and MARK, R. 1967. Fear and the modification of acoustically evoked potentials during conditioning. J. Neurophysiol. 30: 893-910. 15. JANE, J., SMIRNOV, G. and JASPER, H. 1962. Effects of distraction upon simultaneous auditory and visual evoked potentials. Electroenceph. Clin. Neurophysiol. 14: 344-358. 16. JOHN, E. 1967. Electrophysiological studies of conditioning. In G. Guarton, T. Melnechuk and F. Schmitt (ed.), The neurosciences. The Rockefeller Uriiversity Press, New York, p. 690-704. 17. JOHN, E., HERRINGTON, R. and SUTTON, S. 1967. Effects of visual form on the evoked response. Science 155: 1436-1442. 18. KHACHATURIAN, Z. and GLUCK, H. 1969. The effects of arousal on the amplitude of evoked potentials. Brain Res. 14: 589-606. 19. KOSTANDOV, E. 1968. Effect of non-recognized "emotional verbal stimuli" (in Russian). Zh. Vyssh. Nerv. Deyat 18 (3): 371-380. 20. LIFSHITZ, K. 1966. The averaged evoked cortical response to complex visual stimuli. Psychophysiology 3: 55-68. 21. McGINNIES, E. 1949. Emotionality and perceptual defense. Psychol. Rev. 56: 244-251. 22. RITTER, W. and VAUGHAN, H. 1969. Averaged evoked responses in vigilance and discrimination: a reassesment. Science 164: 326-328. 23. SHEVRIN, H. and FITZLER, D. 1968. Visual evoked response correlates of unconscious mental process. Science 161: 295-298. 24. SHEVRIN, H., SMITH, W. and FITZLER, D. 1971. Average evoked response and verbal correlates of unconscious mental processes. Psychophysiology 8: 149-162.
25. SLERRA, G. and FUSTER. J. 1968. Facilitation of secondary visual evoked responses by stimulation of limbic structures. Electroenceph. Clin. Neurophysiol. 25: 274-278. 26. SPERRY, R. 1966. Brain bisection and mechanisms of consciousness. In G. Eccles (ed.), Brain and conscious experience. Springer Verlag. Berlin, p. 298-313. 27. UTTAL, W. 1965. Do compound evoked potentials reflect psychological codes? Psychol. Bull. 64: 377-392. Accepted 27 April 1977 K. KONSTANDOV and Y. ARZUMANOV, Serbsky Central Research Institute of Forensic Psychiatry, Moscow, USSR.