Neuropsychologia, Vol. 16, p. 563to 570. Pergamon PressLtd. 1978. &n&l in GreatBritain
ATTENTION, PREPARATION AND STATISTICAL ASPECTS OF CORTICAL EVOKED POTENTIALS STEVEN R.
SABAT
Department of Psychology, Georgetown University, Washington, DC. 20057, U.S.A. (Received
10 April 1978)
Abstract-Auditory averaged evoked responses @R’s) and associated variance (+ 1.O S.D.) were measured under conditions wherein subjects were alerted, by a warning signal, to respond to a subsequent test signal, and when such preparation was precluded by means of a “shadowing” task. The present tidings indicate that systematic relationships exist between general alertness, focused attention, and strategies of preparation to attend on the one hand, and, on the other, the degree of variance with which neural pools respond. Theoretical implications are explored.
RESEARCH tidings have indicated enhancement of average evoked responses (AER) to attended stimuli and attentuation of AER’s under conditions of distraction [l-4]. These changes in the amplitude of averaged responses have been found to be related to statistical features of the AER, i.e. the variance associated with the averages. Specifically, enhancement of the AER is, under conditions which demand attention, accompanied by decreases in the variance of neuroelectric events, whereas attenuation of the AER under conditions of distraction is accompanied by increased variance in the responses of the neural pool being sampled [5-71.
An hypothesis which has been proposed to account for the observed enhancement of the AER under conditions of attention involves what KARLIN [8] has termed “differential preparation” by the subject before the onset of the relevant stimulus event. In addition, PRIBRAM [9] has theorized that the AER is influenced by prior ongoing slow potential activity. In most studies, the stimulus to be attended to is indicated to the subject and, to test the effects of distraction, the identical stimulus is made “irrelevant” by instructions to the subject to ignore that particular event. Such lack of control in the case of distraction can be precluded quite simply. CHERRY[lo] investigated the effects of a “shadowing” task in which the subject was presented with simultaneous messages to the right and left ears, and told to “shadow” either the right-ear or the left-ear message. Shadowing involved the wordby-word repetition of one of the messages. Under these conditions, subjects were unable to report the contents of the non-shadowed message. Recent research [6] revealed that auditory AER’s to brief clicks presented to either ear were unobservable during the shadowing task. In light of all this, I was interested in determining the effects of preparation and attention upon the variance associated with the AER. In addition, to prevent such preparation under conditions of distraction, a shadowing task was employed and its effects were likewise observed. 563
STEVENR. SABAT
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METHOD Subjects. Three naive college students served as subjects and were asked to shadow one of two unfamiliar messages presented simultaneously and dichotically. Apparatus. Tektronix waveform and pulse generators (160 series) provided a 40 msec “warning signal” of 40 dB intensity followed 2 set later by a 20 msec “test” click of like intensity. The warning signal-test signal package was repeated once every 6 set and presented monaurally. Auditory AER’s to the warning signal and the neuroelectric activity during the foreperiod preceding the test signal were pm-amplified and then amplified by a PAR-142 system with high and low frequency band passes (-3 dB) set at 60 Hz and 0.15 Hz respectively. Evoked responses were then averaged by a Fabri-Tek 1074 signal averager which was slaved to a PDP-8/L digital computer programmed to display the AER waveform and f 1.0 standard deviations around the average. The AER and accompanying variance were displayed on a Tektronix 504 oscilloscope. Shadowed and non-shadowed messages were recorded on separate channels of a Sony TC252D stereo tape-recorder and were delivered through Koss (ESP-6) headphones (response = 27-19,000 Hz f 5 dB). Procedure. Separate monopolar recordings were taken from left and right hemispheres (C3 and C4) using Beckman silver-silver chloride electrodes. Placements were equidistant from the midline and ground leads were attached to each ear. For each subject, warning signal-test signal pairs were presented to the right and then to the left ear in the absence of shadowing. Subjects were instructed to respond to the test signal by pressing a telegraph key as quickly as possible with the right hand. Subjects were then asked to repeat this procedure while shadowing either the left-ear or right-ear message. AER’s and variances were obtained from 65 presentations of the warning signal-test signal package. Eye movements were minimized by requiring subjects to fixate on a designated point.
RESULTS The major findings are shown in Figs. 1 and 2 which represent all three subjects. Figures 1 and 2 present the variance (& 1.O S.D.) of neuroelectric activity in the left and right hemispheres at 200 msec intervals during the foreperiod. The variance associated with the AER to the warning signal (100 msec) is presented as the “control” and the variance at succeeding intervals in presented in terms of percentages of this “control”. Thus, the variance associated with the AER to the warning signal = 100% ; the variance at the conclusion of the foreperiod (2ooO msec) is equal to 52, 57 and 58% of the variance associated
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Fros. 1 and 2. Variance of neuroelectric activity during a 2 set foreperiod, in the left and right hemispheres, associated with the AER to the warning signal presented to the right ear. The variance associated with the AJZR to the warning signal = 100% and is the “Control”. The variance at successive 200 msec intervals during the foreperiod preceding the test signal is expressed as percentages of the “Control”.
with the warning signal for subjects C.W., F.H. and S.V. respectively. Therefore, the variance in the left hemisphere at the conclusion of the foreperiod has decreased by 4842% compared to the variance at the beginning of the foreperiod. For two subjects (C.W. and F.H.) a rather precipitous decrease in neuroelectric variance occurred between 100-800 msec and this level of activity was maintained through the end of the foreperiod. One subject (S.V.) revealed a more gradual decrease in variance over the first 1200 msec of the foreperiod and a more precipitous decrease, from 80 to 58x, during the final 800 msec of the foreperiod. The decrease in neuroelectric variance in the right hemisphere was less abrupt than that occurring in the left hemisphere, yet this decrease, too, is substantial over the entire duration of the foreperiod (48, 44, 42% for subjects C.W., F.H. and S.V. respectively). Thus, the left and right hemisphere reveal asymmetries during the foreperiod, but such asymmetries are not evident at the conclusion of the foreperiod. Figure 3 presents representative waveforms from one subject (C.W.). Each trace begins with the AER to the warning signal and includes the two-second foreperiod preceding the test signal. Separate waveforms were obtained (from left to right) under conditions of (a) warning signal-test signal alone; and (b) shadowing + warning signal-test signal. Under condition (a) the variance associated with the AER to the warning signal systematically decreased as the onset of the test signal approached. Such was true of both the leftand right-hemispheres (top to bottom row respectively) and independent of the ear receiving the warning signal-test signal package. However, under conditions of distraction from the warning signal-test signal pair (b), i.e. during shadowing, the overall variance increased dramatically.
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STEVEN R. SABAT
DISCUSSION The present findings indicate that awareness consists of two distinct, opposing, but interacting, processes akin to WUNDT’S[I l] notions of “Apprehension” and “Apperception”. The former includes all events that “enter into the large region of consciousness” whereas “the elevation into the focus of attention” constitutes apperception. Wundt points out that “The apprehended content is that of which we are more or less darkly . . .” (p, 35). aware; . . . the apperceived Furthermore, “. . . the scope of apperception is a relatively limited and constant one, and the scope of apprehension is not only larger, but also much more variable” (p. 36). Wundt’s notions are, thus, borne out in neuroelectric terms which consist of the decrease in variance which accompanies the focusing of attention, as well as the larger degree of variance characteristic of brain activity at the onset of the warning signal, before attention becomes focused. For all subjects such decreases in variance may be interpreted as increases in the degree of neural synchrony with which the system operates under states of focused attention. Thus, “apprehension” and “apperception” are characterized by levels of neural synchrony which are 4248% higher in the case of the latter, as opposed to the former. For all subjects the preparation to respond to a stimulus is accompanied by a 4248% decrease in the variance of the neuroelectric activity occurring after the warning signal and during the foreperiod leading up to the test stimulus. This result is found in both hemispheres independent of the ear which received the warning signal-test signal ensemble. Thus, as attention becomes focused and as the subject prepares to respond, the synchrony of neuroelectric events increases dramatically. This change in the pattern of neuroelectric responses casts doubt on the notion that enhanced AER’s are due solely to a state of general arousal as has been hypothesized by NAATANEN [ 121.Likewise, the large increase in variance and attenuated AER’s which accompanied shadowing (which, subjects reported, produced high levels of arousal) cast further doubt upon the general arousal notion. Support is found for KARLIN’S[8] theory that, under conditions of attention, enhanced AER’s are due to the subjects’ preparation to respond to the relevant stimulus. Such “preparation” is accompanied by increased synchrony (decreased variance) of neuroelectric events. Earlier research, ROBINSONand SABAT[6] which revealed decreases in AER variance and increased AER amplitudes under conditions of attention, is further informed by the present findings. Specifically, the neuroelectric synchrony which accompanied the AER during states of focused attention has its origins in the subject’s preparation to attend which occurred prior to the onset of the stimulus to be attended. In addition, PRIBRAM’S [9] theory concerning the close relationship between the AER and ongoing slow potential activity finds further support in the present findings. Although the AER may reveal the presence of a signal in the CNS, the structure or distribution of the background noise, upon which the signal is superimposed, determines the degree to which the signal will find representation as revealed in the amplitude of the AER. The development of neuroelectric synchrony under conditions of focused attention follows a time course which is dependent on, and a reflection of, the particular strategy which the subject adopts in preparing to respond to the test signal. In the present experiment, each subject responded to the test signal by depressing a telegraph key with the right hand. The time course of the increase in synchrony in the left hemisphere refIects such strategies, Subjects C.W. and F.H. indicated, following the experiment, that they did not
ATTENTION,
PREPARATION
AND
STATISTICAL
ASPECTS
OF CORTICAL
EVOKED
POTENTIALS
FIG. 3. Auditory AER’s to warning signal from one subject under conditions of (a) Warning signal-test signal and (b) Shadowing + (a). Each separate figure presents the average waveform (center trace) bracketed in (a) above and below by f 1.O standard deviation; and in (b) below by - 1.O standard deviation. Waveforms throughout are the average of 65 presentations of the warning signal-test signal pair to the right ear. The top and bottom rows represent the left and right hemispheres respectively. Time base = 2000 msec foreperiod; polarity convention is negative “up”.
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engage in conscious attempts to count out the duration of the foreperiod prior to their response to test signals. Hence, the rather precipitous, and then maintained decrease in variance. However, subject S.V. indicated that he did, in fact, adopt a “motor set” and attempted to time the two-second foreperiod before responding to the test signal. Hence, the rather gradual decrease in variance over the initial 1200 msec, and then the more precipitous decrease toward the end of the foreperiod when the subject’s attention became focused more fully. The clarity or resolution of our experience of external events as they are sampled will depend upon the degree of attention invested. Such resolution results from the efficiency with which information is processed by the brain and efficiency is expressed in terms of the pre-set synchrony which characterizes the system from moment to moment. The notion that competency in information-processing is reflected in the increased redundancy (reduced equivocation) in the sensory channels [13] thus finds support in the present results. Increased redundancy is reflected in the increased synchrony of responses of neural pools. Thus, as such ensembles respond more synchronously, information processing becomes more efficient, more competent. REFERENCES 1. DA~XS,H. Enhancement of evoked cortical potentials in humans related to a task requiring a decision. Science, N.Y. 145,182-183,1964. 2. SA~~ERFIELD,J. H. Evoked cortical response enhancement and attention in man. A study of responses to auditory and shock stimuli. Electroenceph. Clin. Neurophysiol. 19,470-475,1965. 3. !&NO, P., HAIDER, M. and LINDSLEY,D. B. Selective attentiveness and cortical evoked responses to visual and auditory stimuli. Science, N.Y., 148,395-397,1965. 4. F'ICTON,T. W. and HILLYARD,S. A. Human auditory evoked potentials-II. Bffects of attention. Electroenceph. Clin. Neurophysiol. 36, 191-199, 1974. 5. ROBINSON,D. N. Statistical features of brain responses under conditions of attention and habituation. PsychoI. Rep. 32,287-292, 1973. 6. ROBINSON,D. N. and SABAT, S. R. Elimination of auditory evoked responses under conditions of auditory shadowing. Physiol. Psychol. 3,26-28, 1975. 7. ROBINSON,D. N. and SABAT, S. R. Neuroelectric aspects of information-processing by the brain. Neuropsychologia 15,625-641, 1977. 8. KARLIN, L. Cognition, preparation, and sensory evoked potentials. Psychol. Bull. 73,122-136,197O. 9. PRIBRAM,K. H. Languages ofthe Brain. Prentice Hall, Englewood Cliffs, N.J., 1971. 10. CHERRY,E. C. Some experiments on the recognition of speech with one and with two ears. J. acoust. Sot. Amer. 25,975-979, 1953. 11. WUNDT, W. M. An Introduction ta Psychology. George Allen, London, 1912. (Translated by Rudolf Pintner.) 12. NAATANEN,R. Selective attention and evoked potentials in humans-a critical review. Biol. Psychol. 2, 237-307, 1974. 13. PRIBRAM,K. H. and MCGUINNESS, D. Arousal, activation, and effort in the control of attention. Psycho/. Rev. 82. 116-149 1975.
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Deutschsprachige Zusammenfassung: Gemittdteauditive evozierte Potentiale (ERA) und die entspre. chende Varianz (+ I,0 S. D.) wurden unter Bedingungen gemessen, wo Probanden durch ein Warnsignal darauf vorbereitet wur. den, ein nachfolgendes Testsignal zu beantworten und wenn solcher Vorbereitung mittels einer Scheinaufgabe vorgebeugt wurde. Die bishorigen Ergebnisse zeigen, da!3systematische Beziehungen existieren zwischen allgemeiner Wachheit, gerichteter Aufmerksamkeit und Strategien des Aufmerksamkeit-Vorbereitens einerseits und andererseits dem AusmaB der Varianz, mit dem bestimmte Neuronensysteme antworten. Die theoretischen Folgerungen hieraus werden untersucht.