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Eye movement artifact in the CNV
Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands
EYE MOVEMENT
ARTIFACT
173
IN THE
CNV 1
STEVEN A. HILLYARD AND ROBERT GALAMBOS2
Department of Psychology, Yale University, New Haven, Conn. (U.S.A.) (Accepted for publication: May 14, 1969)
The slow potential shift (Contingent Negative Variation [CNV]) discovered by Walter et al. (1964) appears in human scalp recordings during the preparatory interval between a warning stimulus ($1) and a second stimulus (Se), which either demands a motor response or has motivational values. Extensive subsequent research has shown that the magnitude of the CNV depends upon: (l) stimulus variables, such as intensity of S~ (Irwin et al. 1966; Low et ai. 1967; Rebert et ai. 1967), information content of Se (Walter 1965b; Cohen and Walter 1966), durationofSt-S2interval (Walter 1964; Knott 1969); uncertainty in the delivery of S~ (Walter 1965a; Low 1966), and distraction (Walter et al. 1967; McCallum and Walter 1968; Tecce and Scheff 1969); (2) response variables, such as effort expended (Rebert et al. 1967; Low and McSherry 1968), reaction time (Hiilyard and Galambos 1967; Hillyard 1969a; Tecce and Scheff 1969), response accuracy (McAdam 1966; Hillyard 1969b), subjective concentration (McAdam et aL 1966), delay of response (Walter et al. 1964; Low et al. 1966; Donald 1968), and superimposed tasks (Low and McSherry 1968); and (3) indi. vidual differences, including developmental age (Low 1966; Walter 1966), anxiety index (Knott and Irwin 1967; Low et aL 1967) and psychopathology (Walter 1966; Bostem et al. 1967; McCallum and Walter 1968). Some of these empirical relationships may require re-evaluation in light of the demonstration (Low et al. 1966) that involuntary eye movex This research was supported by U.S. Public Health Service Gr~.nt I.FI-MH-36 and National Institutes of Health Grant GM 01106-03, and formed part of the senior author's doctoral dissertation. s Present address (both authors): Department of Neurosciences, School of Medicine, University of California, San Diego, La Jolla, Calif. 92037.
ments during the S1-S~ interval consistently generated an artifactual, vertex-negative field, having a time course resembling that of the CNV. Low et al. have recorded the CNV from an eyeless patient, but the quantitative extent of the distortion induced in the CNV by ocular potentials in normal subjects has not been determined. In the present study, CNVs were partitioned into an Eye Artifact Potential (EAP) and a "true" or tCN3', presumably of cerebral origin. The EAP amplitudes were ascertained from concurrent DC recordings of the electro-oculogram (EOG), after plotting the relation between EAPs and EOG during voluntary eye movements. METHODS
Subjects
Ten normal young adults each served in one 2-2.5 hour experimental session. None was aware that involuntary eye movements might occur in the CNV situation. Stimuli
Auditory stimuli of moderate intensity were delivered in pairs through earphones; a stimulus pair consisted of a single click (St), followed after 1.30 see, by a 1000 c/sec tone (S~) that could last for 1.21 sec. The time intervals between pre~e,*~ations of successive St-S8 pairs were unpredictably varied. Recording system
Potentials from the eyes and scalp were recorded with Ag-AgCI electrodes (Beckman Instruments). Pairs of electrodes were affixed for recording from: (1) the superior versus the inferior orbital ridge (the vertical electro-oculogram [EOG]); (2) the left versus t,le right outer canthus of the eyes (the horizontal EOG); (3) the vertex Electroenceph. din. Neurophysiol., 19/0, 28:17~-182
! 74
S.A. HILLYARDAND It. GALAMBOS
(C,) versus the right mastoid (the Cz channel); and (4) a site 4 cm anterior to Cz versus the right mastoid (the frontal channel). Electrophysiological potential differences were amplified using Grass 5PI DC pre-amplifiers and were permanently recorded on FM magnetic tape. Off-line response averaging was done with a Fabri-tek 1052 computer.
Experimental procedure
The magnitudes of EAP and tCNV could be calculated, after obtaining an equal number of trials with mirror images "upward" eye rotations of the same extent. Ten to 12 trials each of upward and downward rotations were carried out~ with dots separated by 2.5, 5, 7.5, 10 and 15° of visual arc. These angles were chosen so that the resulting EOG deflections would extend over the domain of EOG shifts encountered during the S1-S~-respond condition. Upward and downward rotations of 10° were repeated in three subjects, under instructions to "try very hard to make the (return) eye movement to $2 as fast as you can". This is referred to as the "high effort" condition, all previous rotations having been made under "low effort".
The subject was seated in an easy chair, with head and neck resting against the back. The three experimental treatments were then administered in the following order: Control condition (no response). The subject was instructed to remain motionless with eyes closed while 16 $1-$2 pairs were delivered, with inter-pair intervals ranging between 6 and 16 sec. Analysis of tape-recorded data Potential shifts were computer-averaged over These trials acquainted him with the S1-Sa pairing, ensuring that CNVs would rapidly ascend to an epoch of 4.096 sec, beginning 0.50 sec before full amplitudes (Hillyard and Galambos 1967). the delivery of S1, and the averaged wave forms S1-S~-respondcondition. Next, he was informed were written out on an X-Y plotter. The amplithat the click-tone stimulation would continue tude of an averaged CNV or EOG deflection was as before, and was ordered to respond to S~ designated as the mean potential level during the by pressing a thumb-actuated lever"as fast as you 0.3 sec interval preceding the onset o/' Sz, relative can". Between 100 and 150 S1-S2-respond trials to the DC baseline established during the halfwere then administered, with a mean inter-trial second period before 51. interval of 17 sec. Six subjects performed these Analysis of Sl-$2-respond trials. Potential trials with the eyes closed, while the other four shifts in the scalp and EOG channels were avermaintained visual fixation upon a central dot aged and quantified in blocks of eight consecuduring the latter half of the trials. tive trials each. By referring to the EAP-EOG Voluntary eye movements. This procedure was regression functions (described below) each averdesigned to establish the function relating the aged CNV was broken down into its EAP and amplitude of the EAP to that of the concurrent tCNV compone,,ts. potential shift in the EOG. The relationship of the CNV to eye moveDirectly in front of the subject's chair was a ments was further specified by averaging CNVs white screen, upon which a pair of mobile, one- from eyes-closed trials in blocks of 12, grouped degree "dots" was placed to serve as fixation together on the basis of the size of the EOG depoints. One dot was placed at eye level on the flection. In three subjects, trials were divided into central vertical meridian and the second dot was those 12 with the largest (most negative) EOG depositmned directly below it, separated by a speci. flections, those having the 12 next-largest, and so fled visual angle. The subject fixated his eyes on on, down to those 12 with the smallest (most posithe upper dot and was told to shift his gaze to the tive) deflections. lower dot upon hearing the first member of an Analysis of voluntary eye movement trials. St-S~ pair, and to redirect and sustain fixation Eight trials with uniform and well-shaped EOG back to the upper dot when Sa began. deflections were selected from each condition, The CNVs produced during these movements and the potential shifts induced in all channels contained a "square-wave" EAP component, were computer.averaged and quantified. A supspreading from the corneo-retinal field, plus a plemental measurement was made at an earlier tCNV preceding the ocular motor response to S2. point in the S~-$8 interval, thus doubling the
Electroenceph.clin. Neurophysiol.,1970,28:173-182
EYE MOVEMENTSAND CNV UPWARD
DOWNWARD
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Fig. Computer-averaged potential shifts produced simultaneously in the three channels by upward (left) and downward (righO rotations of the eyes in response to Sh with return rotations after S#. Dot separation is 10°. Upward deflections from baseline signifynegativity in frontal, Cz, and upper orbital leads, respectively. Numbers shown are quantified potential shifts(in ~uV).Time calibration in this and subsequent figuresis 1.30sec between St and onset of $2.
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Fig. 2 Top: Idealized wave forms of EAP produced in a scalp channel during downward (B) and upward (6"3voluntary eye rotation. The tCNV (A) is the same for rotations in either direction. Bottom: Heavy lines represent idealized wave forms of CNVs in a scalp channel during downward (D) and upward (£) eye rotations. The shift labeled D is formed by adding components A and B, and the shift at E is the sum of components A and C. number of data points for defining the EAP-EOG function. RESULTS Voluntary eye movements Fig. 1 shows typical examples of CNVs and concomitant EOG deflections generated during u p w a r d and downward eye rotations of 10°. Negative CNVs were produced in the scalp channels during downward rotations, due to elevation
175
of the negative, posterior end of the corneo-retinai dipole, while positive CNVs accompanied upward eye displacements. The negative CNV of such a pair was larger in amplitude than the positive one, because the negative EAP caused by downward eye movement added with the concurrent tCNV, while the positive EAP (upward rotation) was partially cancelled out by the tCNV. The amplitudes of the EAP and tCNV could be calculated from raw data such as these, using the additive model, shown geometrically in Fig. 2. Each of the idealized CNVs shown at the bottom of Fig. 2 is the sum of an EAP, which is negative for downward and positive for upward eye rotations, plus a negative tCNV that precedes the ocular response to $9. The tCNVs are assumed to be identical for rotations made in either direction. The tCNV amplitude can be calculated simply by adding the pair of CNVs recorded during upward and downward rotations of equal extent; the EAPs cancel out and the sum represents twice the tCNV amplitude. Conversely, subtraction of the "downward" CNV from the "upward" one eliminates the tCNVs, leaving twice the EAP as the remainder. The subject of Fig. 1, V~ikeseveral others, exhibited vertical EOG deflections that were 2030% larger (absolutely) during downward eye movements than during upward ones. This disparity was tentatively attributed to differences in the extents of upward and downward rotationsL Such disparities would engender different-sized x The factors responsible for this commonly observed disparity of 20--30~ between EOG deflectionduring up. ward versus downward voluntary rotations were not identified with certitude. The most likely explanation is that subjects made systematicerrors of fixation,such that angular displacementsmade during the downward movements were absolutely larger; this could have resulted from the dots not beingexactly at the levelof the resting eye. However, a unidirectional shifting of the EOG electrodes in relation to the eye could have produced the ~me discrepancy. In the latter case, however,the EOG would not have borne a one-to-one relation with eyeball position relative to the skull, whichdeterminesthe EAP, and, therefore, the EAP-EOG functions would have been inaccurate. To rule out such an error, independent evidencewas presented for four subjects (Fig. 8) to show that the regressionfunc*.ions had made accurateand valid partitions. In the remaining subjects, however, their accuracy was not directlyverified; such would depend both upon the invarianceof the relation between the EOG and eye position, and the constancy of the tCNV during upward and downward rotations. Electroencep~. olin, NeitrophysioL, 1970, 28:173-182
! 76
S. A. HILLYARD AND R. GALAMBOS
EAPs, and this was accounted for by linear interpolations in the calculations, a sample of which foiiows: Using the data portrayed in Fig. I, the mean amplitude of EAP in the Cz channel is given by:
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EAP = [19.6 - - ( - 34.0)]/2 = 26.8 pV in conjunction with a mean EOG deflection during these rotations of: EOG deflection- [138 - - ( - 175)]/2= 157 pV Such concurrent pairs of EAPs and EOG deflections produced at the different angles of dot separation are plotted for four subjects in Fig. 3. These EAP-EOG functions are graphed in terms of absolute amplitudes, because they apply to EAPs generated by either upward or downward eye movements. The growth of EAP with increasing EOG deflection was linear in all subjects, and the leastsquares method was used to obtain the lines of best fit. The strength of the linear relation is indicated by the statistic r 2, the square of the productmoment correlation. The parameters of the reII0
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[POTENTIAL SHIFT IN EOO] (pV) Fig. 3 Linear increase of eye movement artifact (EAP) in Cs (open circles) and frontal (solid circles) channels with increasing EOG deflections, all simultaneously induced by voluntary eye rotation. Absolute values indicate that the EAP and EOG deflection may be of either polarity. The least-squares regression lines and their slopes (b) and inter. cepts (a) for the C,, channel are given for each of the four subjects.
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'Low' 'High' RESPONSEEFFORt" Fig. 4 Three-fold increase in tCNV brought about by enacting the return eye movements to S2 with greater speed and effort. Average of three subjects; dot separation is 10°.
gression lines did not differ significantly amo,g subjects. The rate of increase of EAP in the frontal channel was significantly steeper than in the Cz channel. Presumably, more artifact was induced in the frontal electrode per unit increment in the ocular field shift because this site was closer to the eyes. These EAP-EOG relationships were found to be invariant with large changes in initial eye position, thus ensuring their applicability to the Si-S~-respond condition, wherein initial eye position was not controlled. tCNV preceding voluntary eye movemenl~, The mean tCNV during the 0.3 sec before S~ ranged between - 0 . 4 and -21.3 pV, with an over-all mean of - 5.9 pV on all trials enacted under "low effort" conditions. Analysis of variance showed that there was no effect of the size of eye move. ment upon the amplitude of the tCNV. The tCNV was greatly augmented when the ocular response to Ss was made with"high effort" (rapid response) in three subjects. The m~an tCNV was incremented from - 4 . 8 ~V, for low effort rotations of l0 °, to - 16+0pV, a highly significant increase (F(l,9)-- 15.81,P < 0.01) (Fig. 4). Although increasing the speed of the return response greatly enhanced the tCNV, the EAP produced by these l0 ° displacements remained Eiectroenceph. clin. Neurophysiol., 1970, 2.8:173-182
177
EYE MOVEMENTS AND CNV
unchanged. The tCNV could thus be increased independently from the EAP, whereas the EAP could be independently enlarged by making bigger eye movements. This demonstrates the existence of two additive, separable components in the CNV, one determined by response effort and the other by ocular displacement.
Synchronized with the CNV was a consistent potential shift in the EOG, reflecting a pattern of involuntary eye movement. Fig. 5 shows typical CNVs and simultaneously rvcorded EOGs from nine subjects. The most common EOG wave form was a large negative shift (downward eye rotation) that peaked near the onset of Ss and bore a disturbing resemblance to the scalp-recorded CNV. In other subjects, however, the EOG deflections were very small, or even positive for part of the St-Ss interval. Lateral eye movements, as indexed by the horizontal EOG, were invariably too small to contribute artifact to the scalp channels and will not be considered further. Although each subject exhibited an idiosyncratic pattern of eye movements, there was substantial trial-to-trial variation in the quantified magnitude of the EOG deflection, which introduced considerable variability into the CNV. Using each individual's regression function (as in Fig. 3), the averaged CNVs were algebraically segregated into EAP and tCNV components; the trial-to-trial variation of these potentials within two subjects is shown in Fig. 6. The right hand
Control trials When no motor responses were made, the potential shift in the Cz channel within the 0.3 sec preceding Ss was within noise levels, averaging - 0 . 5 pV over all subjects on the 16 trials. The mean deflection in the EOG was also negligible. Si-S~-respond trials When lever presses were made at the onset of Ss, large CNVs developed in both C,~ and frontal channels within the first few trials. Each subject displayed a distinctive CNV wave form that was recognizable from one block of trials to the next, but varied considerably in amplitude. The mean CNV (Cz channel) from all trials ranged between - 16.2 and - 38.6/tV in different subjects.
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Fig. 6 Spontaneous variation in the CNV and its two components, EAP and tCNV (vertically hatched area), averaged over successive blocks of eight trials with the eye~ closed in two subjects. The number assigned to each block is the percentage of the CNV that was constituted by EAP on those trials.
column of Table l gives the range of EAPs exhibited by each subject on different blocks of trial~, In the five subjects with large EAPs (aver. aging more than 25°/,, of the CNV), there was a higher correlation of EAP with CNV amplitude (average Pearson r=0.72) than of tCNV with CNV amplitude (average r=0.31). This means that the ocular artifact could contribute more to the variance of the CNV than did the "cerebral" component. In general, tCNV amplitudes were independent of the size of the EAP, even in subjects making large eye movements. The mean amplitudes over all trials of CNV, EAP and tCN~', in C~ and frontal channels, and the mean per cent EAP/CNV are presented in Table [ for each subject. On the average across all subj~ts, -6.4 pV or 23% of the CNV was corn. posed of artifact, resulting from a net tendency to move the eyes downward during the $1-58 interval when the eyes were closed.
Validity of the partition of CNV. CNVs from three subjects were computer-averaged in blocks of 12, grouped together on the basis of the size of the EOG deflections. This procedure produced pairs of averaged responses like those in Fig. 7, making conspicuous the dependence of CNV upon the EOG deflection. The growth of CNV with increased EOG deflection confirms that the latter potential shift was actually caused by an ocular rotation that engendered an electric field at the scalp, rather than by movement of the EOG electrodes or some other localized process. Furthermore, this dependence of CNV upon the EOG deflection was linear, with a slope that was usually identical to that of the EAP-EOG function. The final demonstration of the validity of dividing the CNV into tCNV and EAP components is based upon data obtained from four subjects, during S1-S~-respond trials enacted with the eyes fixed on a target. Representative CNVs and concomitant EOGs from these subjects are shown in Fig. 8. In each case a substantial CNV was evident in the absence of any ocular deviation, and, therefore, consisted of tCNV. The mean tCNV from these subjects, measured over 200 eyes-fixated trials, was - 21.4pV in the Czchannel. The mean tCNV calculated from 250 separate eyes-closed trials in the same subjects was -22.9 pV. In the frontal channel, the mean tCNV was -13.0/~V on eyes-fixated trials and was calculated to be -13.4 pV on eyes-closed trials. The correspondence between these magnitudes demonstrates the accuracy of the partition of CNV by the regression function. DISCUSSION
A significant proportion of the CNV in most subjects was comprised of electric fields spreading passively from the corneo-retinal dipole, which was rut~ted involuntarily during leverpressing trials when the eyes were closed. On the average, across all subjects, -6.4/~V or 230/0 of the CNV was composed of artifact, but the EAP often reached - 10 to - 20/~V, due to systematic, downward eye rotations synchronized to the task. In fact, in those subjects whose eye movements were large, the EAP contributed more to the variance of the CNV than did the "cerebral" component. Electroenceph. din. Neurophysiol., 1970, 28:173-182
179
EYE MOVEMENTS AND CNV
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TABLE 1 Mean amplitude of CNV and its components (in/~V) for each subject during St-Sa-respond trials with eyes closed CNV
EAP
tCNV
EAP/CNV (per cent)
Range of EAP amplitudes*
EIO MeG COL CQK WOW LZO WRG GUS FOU CLY
--25.3 -29.7 --37.5 -38.6 -28.4 --29.5 -- 16.2 --25.1 --23.4 --18.8
- 6.9 + 2.9 -12.7 - 5.8 - 10.8 - 1.7 -- 1.4 -- 4.2 --17.8 -- 5.6
- 18.4 -32.6 -24.8 -32.8 - 17.6 -27.8 -- 14.8 --20.9 -- 5.6 --13.2
27 -10 33 15 38 6 9 t7 76 30
+ 6,0, - 18.0 + 1 0 . 5 , - - 6.3 -- 5 . 0 , - 3 9 . 8 0 ,9.5 - 0.8, - 2 0 . 5 -- 0 . 6 , - 2.5 + 0.9, -- 5.0 -- 1 . 6 , - 5.6 --12.0,--24.9 -- 0 . 1 , - - 1 0 . 6
Mean
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* These are maximum negative and positive EAPs that were observed when responses were averaged in blocks of eight sequential trials.
Electroenceplt. clin. Neurophyslol., 19'/0, 28:173-182
180
S.A. HILLYARD A N D R. G A L A M B O S
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CNV--~ I Fig. 8 CNVs recorded from Cz channel and the concurrent EOGs from four subjects, averaged ovvr one block of S1-S~-respond trials while the eyes were fixated upon a central target. Large positive waves in the EOG were caused by eye-blinks following S~. Calibrations: CNV = 20pV; EOG = 100pV.
In some of the earlier studies cited above, correlations were observed between small changes in CNV amplitude (of 5-10 pV) and various stimulus and behavioral variables. In many cases such •/ariation could have resulted from changes in eye movement patterns instead of changes in a brain potential. If the size of eye movements happened to covary with a particular behavioral variable, an oculomotor-behavioral relationship might be misinterpreted as an electrocerebral-behavioral one. Most of the more recent investigations, however, have displayed an awareness of the ocular contamination problem and have controlled for it with more or less rigor by one of the techniques described below. The simplest and most reliable way to isolate the tCNV from ocular potentials was found to be .~.recording with the eyes fixated on a point, which generally eliminated slow eye movements. A more complicated but equally valid technique was the estimation of EAP magnitudes by concurrent recording of the calibrated vertical EOG. Walter (1967) has described a third method for attenu. ating this artifact from scalp recordings; the reference lead was attached to a potentiometer, which balanced the resistance between a linked mastoid and a supra-orbital electrode, so that EAPs induced at the vertex and at the virtual reference were equal. The validity of this method would seem to depend upon a linear relation between potential shifts in the reference lead andEAPs at the vertex, which is substantiated by the iinearity of the present EAP-EOG functions. A
final method, indirect though acceptable if carefully quantified, was to show that eye movements are equal in size under different experimental conditions (Tecce and Scheff 1969). The distribution of potential shifts induced across the scalp by eye movements and blinks has been plotted previously (Zao et al. 1952; Peters 1967), but not for displacements of much less than 10°, which demands the use of computer averaging techniques and segregation of the con. founding tCNVs. Rowland (1968), however, has cited reports that "small" voluntary movements can cause DC artifacts that decline in amplitude with distance from the eye, but are clearly present even at the oc~iput; he also reported that in half of the subjects, CNV recordings were severely contaminated by such artifact, even during attempted visual fixation. Cant et aL (1966) also discovered that eye movements must be excluded before DC shl~'ts of cerebral origin could be assessed, particularly when complex visual stimuli were used. These findings suggest that the later components of scalp evoked potentials could also suffer ocular contamination if an eye blink or "twitch" was evoked by the stimulus. Goffet al. (1969) have identified such artifacts in the evoked potentials on the human scalp, but found their spatial distributions limited to frontal regions. Nonetheless, it is possible that certain individuals or manipulations (Rietveld 1966) may produce large, phasic eye displacements which would influence more posterior recording sites. Electroenceph. clin. Neurophysiol., 1970, 28:173-182
EYE M O V E M E N T S A N D C N V
The tCNV was found to be independent from the EAP in both lever-pressing and voluntary eye-moving tasks. The tCNV preceding voluntary eye movement was enhanced by increasing response speed and effort, while in thelever-pressing task the tCNV was often correlated with reaction time (Hillyard 1969a). The correspondence of the tCNV with such response dimensions supports the thesis that it is a response-governirtg brain potential, associated with the psychological constructs of preparatory set, response selection (Donald 1968) and conation (Low et al. 1966). SUMMARY
During the preparatory interval between a warning click and a tone burst that signalled a lever press, a slow negative potential shift (CNV) was recorded from the scalp in ten normal adults. When the eyes were closed, involuntary eye movements during the click-tone interval consistently generated potential shifts which spread from the corneo-retinal dipole to the scalp electrodes and thereby contaminated the CNV. The CNV was quantitatively partitioned into an artifactual component caused by ocular rotation (the EAI ), which summated with the second component, presumably of cerebral origin, called the "true" or tCNV. The EAP amplitudes were estimated from concurrent recordings of the electro-oculogram. In the average subject, 23% or -6.1/~V of the total CNV was comprised of EAP, and the EAP often reached from - 1 0 to - 1 5 /~V. The accuracy of the partition was verified by comparing tCNVs recorded with eyes closed and with eyes immobilized by fixation. The CNV produced during voluntary eye movements was similarly divided into a tCNV, which was tripled in amplitude when ocular responses were made with increased speed and effort, and an EAP, which was determined solely by the amount of ocular displacement.
R~SUM~ ART~,FACTDO AUX MOUVEMENTSDES YEUX DANS LA VARIATION CONTINGENTE NI~GATIVE
Au cours de l'intervalle pr6paratoire entre un clic d'avertissement et une s~rie de sons qui constitue le signal de presser un levier, un potentiel n~gatif lent (VCN) est enr©gistr~ au niveau de
181
scalp chez dix adultes normaux. Lorsque les yeux sont ferm6s, des mouvements involontaires des yeux darts l'intervalle entre le clic et les bruits produisent de fro;on constante des variations de potentiel qui diffusent du dipole corn6o-r6tinien attx ~lectrodes de scalp et ainsi contaminent la VCN. La VCN se r6partit quantitativement en une composante artffactielle caus6e par la rotation oculaire, qai s'additionne ~tla seconde composante probablement d'origine c~r6brale, appel6e la v6ritable variation contingente n6gative (VVCN). Les amplitudes de la composante artffactielle peuvent 8tre appr6ci6.es /i partir d'enregistrements simultan6s d'61ectro-oculogrammes. En moyenne, 23% ou -6.1 /~V de la VCN totale consiste en potentiels artffactiels qui atteignent souvent de - 10/t - 15/IV. La pr~ision de cette r6partition est v6rifi6e en comparant les vraies variations contingentes n6gatives enregistr~es les yeux ferm~s et les yeux immobilis6s par fixation. La VCN provoqu6e pendant les mouvements oculaires vo~ontaires sont de meme divis6s en une vraie variation contingente n6gative, qui est tripl6e en amplitude quand les r6ponses oculaires se font avec une vitesse et un effort accrus, et une composante artffactielle qui n'est due qu'~ ia quantit6 de d~placement oculaire. ,,
REFERENCES BOSTEM, F., ROUSSS'AU, M. C., DF.GOSSEL¥, M. and DONGIF.R, M. Psychopathological correlations of the non-specific portion of visual and auditory evoked potentials and the associated contingent negative variation. Electroenceph. olin. Neurophysiol., 1967, Suppl. 26: 131-138. CANT, a. R., PEARSON,J. E. and BICKFORD,R. G. The mechanism of the expectancy wave in man. Electroenceph, din. Neurophysiol., 1966, 21: 619--620. COHEN, J. and WALTER, W. G. The interaction of responses in the brain to semantic stimuli. Psychophysiology, 1966, 2: 187-196. DONALD, M. W. Electrocortical correlates of fixed.fore. period decision tasks. Unpublished doctoral dissertation: McGill University, Montreal, February 1968. GOFF, W. R., MATSUMIVA,Y., ALLISON,T. and Govv, G. D. Cross-modality comparisons of averaged evoked potentials. In E. DONCmN and D. B. LtNVSLEV(Eds.),
Averaged evoked potentials: methods, results, evalu. ations. NASA SP-191, Washington, D.C., 1969. HILLVARD, S. A. Relationships between the contingent negative variation (CNV) and reaction time. Physiol. Behav., 1969a, 4: 351-358.
Electroenceph. clin. Neurophysiol., 1970, 28:173-182
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s. A. HILLYARD AND R. GALAMBOS
movements. Amer. J. EEG Technol., 1967, 1: 27--40. HII.LYARD,S. A. The CNV and the vertex evoked potential during signal detection, in E. DONCHIN and D. B. REBVJ~T, C. S., MCADAM, D. W., KNOTT, J. R. and IRWIN,D. A. A slow potential change in human brain LIN~LE¥ (Eds.), Averaged evoked potentials : methods, related to level of motivation. J. comp. physiol. results, evaluations. NASA SP-191, Washington, D.C., Psychol., 1967, 63: 20-23. 1969b. HILLYAgD,S. A. and GALAMBOS,R. Effects of stimulus RIETVELD,W. J., Tom3om, W. E. M. and HAGENOUW, J. R. B. Influence of attentiveness, of vigilance task and response contingencies on a surface negative difficulty and of habituation on cortical evoked slow potential shift in man. Electroenceph. elin. responses and on artifacts. Acta physiol, pharmacoi. Neurophysiol., 1967, 22: 297-304. neerl., 1~6, 14: 18--37. IRWIN,D. A., KNOtt, J, R., MCADAM,D. W. and R~BERT, C. S. Motivational determinants of the "contingent ROWLAND, V. Cortical steady potential (direr-current potential) in reinforcement and learning. Progress negative variation". Eiectroenceph, clin. Neurophysiol., physiol. Psychoi., 1968, 2: 1-77. 1966, 12: 538-543. T~ccE, J. J. and SCH~FF,N. M. Attention reduction and KNOTT, J. R. In M. DONOIEn(Ed.), Variation contingente suppressed direct.current potentials in the human brain. ndgative University of Lii~ge,Press, Liege, 1969. Science, 1969, 164: 331-333. KNOTT, J. R. and IRWIN, D. A. Anxiety, stress, and the contingent negative variation. Eiectroenceph. clin. WALTElt,W. G. Slow potential waves in the human brain associated with expectancy, attention and decision. Neurophysioi., 1967, 22: 188. Arch. Psychiat. Nervenkr., 1964, 206: 309-322. Low, M. D. An electroencephalographic correlate of conative states. Doctoral dissertation: Baylor Uni- WALTER, W. G. Effects on anterior brain responses of an expected association between stimuli. Psychosom. versity, Ann Arbor, Mich.; University Microfilms, No. 66.11,848, 1966. Res., 1965a, 9: 45-49. Low, M. D., BORDA,R. P., FROST,J. D. and KeLLAW^Y, WALTER, W. G. Brain responses to semantic stimuli. P. Surface-negative slow potential shift associated Psychosom. Res., 1965b, 9: 51-61. with conditioning in man. Neurology (Mlnneap.), WAL't~R, W. G. Electrophysiologic contributions to 1966, 16: 771-782. psychiatric therapy. Curr. psychiat. ?'her., 1966, 6: Low, M. D., COATES,A. C., RETTIO,G. M. and MCSHERaY, 13-25. J. W. Anxiety, attentiveness.alertness: a phenomeno- WAL~n, W. G. Slow potential changes in the human logical study of the CNV. Neuropsychologla, 1967, .~: brain associated with expectancy, decision and in379-384. tention. Electroenceph. clin. Neurophyslol., 1967, Suppl. Low, M. D. and McSxERRV, J. W. Further observations 26: 123-129. of psychological factors involved in CNV genesis. WALTER,W. G., COOPER,R., ALDRIDOE,V. J., MCCALLUM, Eiectroenceph. clin. Neurophysiol., 1968, 25: 203-207. W. C. and WINTER,A. L. Contingent negative variaMeAD^M, D. W. Slow potential changes recorded from tion: an electric sign of sensory-motor association and human brain during learning of a temporal interval. expectancy in the human brain. Nature (Load,), Psychon. Sci., 1966, 6: 435-436. 1964, 203: 380-384. MCADAM,D. W., IRWIN,D. A., REgEnT,C. S. and KNOTT, WALTER, W. 0., COOPER,R., CROW, H. J., MCCALLUM, J. R. Conative control of the contingent negative W. C., WARREN,W. J., At t~mDeE, V. J., STORMVAN variation. Electroenceph, clin. Neurophysiol., 1966, 2: LEEUWEN, W. and KAMP, A. Contingent negative 194-195. variation and evoked responses recorded by radioMCCACLUM, W. C. and WALTER,W. G. The effects of telemetry in free-ranging subjects, glectroeneeph, din. attention and distraction on the contingent negative Neurophysiol., 1967, 23: 197-206. variation in normal and neurotic subjects. Electro, ZAO, Z. Z., GELniN, M., et R~MOND, A. Le champ enceph, clin. Neurophysiol., 1968, 25: 319-329. 61ectrique de l'oeil. Sem. HOp. Paris, 1952, 28 (36): I ~ R S , J. F. Surface electrical field generated by eye I-8.
Reference: HILLYARD,S. A. and GALAMBOS,R. Eye movement artifact in the CNV. Electroenceph. olin. Neurophysiol., 19"1C,28: 173-182,
EYE MOVEMENT
ARTIFACT
173
IN THE
CNV 1
STEVEN A. HILLYARD AND ROBERT GALAMBOS2
Department of Psychology, Yale University, New Haven, Conn. (U.S.A.) (Accepted for publication: May 14, 1969)
The slow potential shift (Contingent Negative Variation [CNV]) discovered by Walter et al. (1964) appears in human scalp recordings during the preparatory interval between a warning stimulus ($1) and a second stimulus (Se), which either demands a motor response or has motivational values. Extensive subsequent research has shown that the magnitude of the CNV depends upon: (l) stimulus variables, such as intensity of S~ (Irwin et al. 1966; Low et ai. 1967; Rebert et ai. 1967), information content of Se (Walter 1965b; Cohen and Walter 1966), durationofSt-S2interval (Walter 1964; Knott 1969); uncertainty in the delivery of S~ (Walter 1965a; Low 1966), and distraction (Walter et al. 1967; McCallum and Walter 1968; Tecce and Scheff 1969); (2) response variables, such as effort expended (Rebert et al. 1967; Low and McSherry 1968), reaction time (Hiilyard and Galambos 1967; Hillyard 1969a; Tecce and Scheff 1969), response accuracy (McAdam 1966; Hillyard 1969b), subjective concentration (McAdam et aL 1966), delay of response (Walter et al. 1964; Low et al. 1966; Donald 1968), and superimposed tasks (Low and McSherry 1968); and (3) indi. vidual differences, including developmental age (Low 1966; Walter 1966), anxiety index (Knott and Irwin 1967; Low et aL 1967) and psychopathology (Walter 1966; Bostem et al. 1967; McCallum and Walter 1968). Some of these empirical relationships may require re-evaluation in light of the demonstration (Low et al. 1966) that involuntary eye movex This research was supported by U.S. Public Health Service Gr~.nt I.FI-MH-36 and National Institutes of Health Grant GM 01106-03, and formed part of the senior author's doctoral dissertation. s Present address (both authors): Department of Neurosciences, School of Medicine, University of California, San Diego, La Jolla, Calif. 92037.
ments during the S1-S~ interval consistently generated an artifactual, vertex-negative field, having a time course resembling that of the CNV. Low et al. have recorded the CNV from an eyeless patient, but the quantitative extent of the distortion induced in the CNV by ocular potentials in normal subjects has not been determined. In the present study, CNVs were partitioned into an Eye Artifact Potential (EAP) and a "true" or tCN3', presumably of cerebral origin. The EAP amplitudes were ascertained from concurrent DC recordings of the electro-oculogram (EOG), after plotting the relation between EAPs and EOG during voluntary eye movements. METHODS
Subjects
Ten normal young adults each served in one 2-2.5 hour experimental session. None was aware that involuntary eye movements might occur in the CNV situation. Stimuli
Auditory stimuli of moderate intensity were delivered in pairs through earphones; a stimulus pair consisted of a single click (St), followed after 1.30 see, by a 1000 c/sec tone (S~) that could last for 1.21 sec. The time intervals between pre~e,*~ations of successive St-S8 pairs were unpredictably varied. Recording system
Potentials from the eyes and scalp were recorded with Ag-AgCI electrodes (Beckman Instruments). Pairs of electrodes were affixed for recording from: (1) the superior versus the inferior orbital ridge (the vertical electro-oculogram [EOG]); (2) the left versus t,le right outer canthus of the eyes (the horizontal EOG); (3) the vertex Electroenceph. din. Neurophysiol., 19/0, 28:17~-182
! 74
S.A. HILLYARDAND It. GALAMBOS
(C,) versus the right mastoid (the Cz channel); and (4) a site 4 cm anterior to Cz versus the right mastoid (the frontal channel). Electrophysiological potential differences were amplified using Grass 5PI DC pre-amplifiers and were permanently recorded on FM magnetic tape. Off-line response averaging was done with a Fabri-tek 1052 computer.
Experimental procedure
The magnitudes of EAP and tCNV could be calculated, after obtaining an equal number of trials with mirror images "upward" eye rotations of the same extent. Ten to 12 trials each of upward and downward rotations were carried out~ with dots separated by 2.5, 5, 7.5, 10 and 15° of visual arc. These angles were chosen so that the resulting EOG deflections would extend over the domain of EOG shifts encountered during the S1-S~-respond condition. Upward and downward rotations of 10° were repeated in three subjects, under instructions to "try very hard to make the (return) eye movement to $2 as fast as you can". This is referred to as the "high effort" condition, all previous rotations having been made under "low effort".
The subject was seated in an easy chair, with head and neck resting against the back. The three experimental treatments were then administered in the following order: Control condition (no response). The subject was instructed to remain motionless with eyes closed while 16 $1-$2 pairs were delivered, with inter-pair intervals ranging between 6 and 16 sec. Analysis of tape-recorded data Potential shifts were computer-averaged over These trials acquainted him with the S1-Sa pairing, ensuring that CNVs would rapidly ascend to an epoch of 4.096 sec, beginning 0.50 sec before full amplitudes (Hillyard and Galambos 1967). the delivery of S1, and the averaged wave forms S1-S~-respondcondition. Next, he was informed were written out on an X-Y plotter. The amplithat the click-tone stimulation would continue tude of an averaged CNV or EOG deflection was as before, and was ordered to respond to S~ designated as the mean potential level during the by pressing a thumb-actuated lever"as fast as you 0.3 sec interval preceding the onset o/' Sz, relative can". Between 100 and 150 S1-S2-respond trials to the DC baseline established during the halfwere then administered, with a mean inter-trial second period before 51. interval of 17 sec. Six subjects performed these Analysis of Sl-$2-respond trials. Potential trials with the eyes closed, while the other four shifts in the scalp and EOG channels were avermaintained visual fixation upon a central dot aged and quantified in blocks of eight consecuduring the latter half of the trials. tive trials each. By referring to the EAP-EOG Voluntary eye movements. This procedure was regression functions (described below) each averdesigned to establish the function relating the aged CNV was broken down into its EAP and amplitude of the EAP to that of the concurrent tCNV compone,,ts. potential shift in the EOG. The relationship of the CNV to eye moveDirectly in front of the subject's chair was a ments was further specified by averaging CNVs white screen, upon which a pair of mobile, one- from eyes-closed trials in blocks of 12, grouped degree "dots" was placed to serve as fixation together on the basis of the size of the EOG depoints. One dot was placed at eye level on the flection. In three subjects, trials were divided into central vertical meridian and the second dot was those 12 with the largest (most negative) EOG depositmned directly below it, separated by a speci. flections, those having the 12 next-largest, and so fled visual angle. The subject fixated his eyes on on, down to those 12 with the smallest (most posithe upper dot and was told to shift his gaze to the tive) deflections. lower dot upon hearing the first member of an Analysis of voluntary eye movement trials. St-S~ pair, and to redirect and sustain fixation Eight trials with uniform and well-shaped EOG back to the upper dot when Sa began. deflections were selected from each condition, The CNVs produced during these movements and the potential shifts induced in all channels contained a "square-wave" EAP component, were computer.averaged and quantified. A supspreading from the corneo-retinal field, plus a plemental measurement was made at an earlier tCNV preceding the ocular motor response to S2. point in the S~-$8 interval, thus doubling the
Electroenceph.clin. Neurophysiol.,1970,28:173-182
EYE MOVEMENTSAND CNV UPWARD
DOWNWARD
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Fig. Computer-averaged potential shifts produced simultaneously in the three channels by upward (left) and downward (righO rotations of the eyes in response to Sh with return rotations after S#. Dot separation is 10°. Upward deflections from baseline signifynegativity in frontal, Cz, and upper orbital leads, respectively. Numbers shown are quantified potential shifts(in ~uV).Time calibration in this and subsequent figuresis 1.30sec between St and onset of $2.
A.
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Fig. 2 Top: Idealized wave forms of EAP produced in a scalp channel during downward (B) and upward (6"3voluntary eye rotation. The tCNV (A) is the same for rotations in either direction. Bottom: Heavy lines represent idealized wave forms of CNVs in a scalp channel during downward (D) and upward (£) eye rotations. The shift labeled D is formed by adding components A and B, and the shift at E is the sum of components A and C. number of data points for defining the EAP-EOG function. RESULTS Voluntary eye movements Fig. 1 shows typical examples of CNVs and concomitant EOG deflections generated during u p w a r d and downward eye rotations of 10°. Negative CNVs were produced in the scalp channels during downward rotations, due to elevation
175
of the negative, posterior end of the corneo-retinai dipole, while positive CNVs accompanied upward eye displacements. The negative CNV of such a pair was larger in amplitude than the positive one, because the negative EAP caused by downward eye movement added with the concurrent tCNV, while the positive EAP (upward rotation) was partially cancelled out by the tCNV. The amplitudes of the EAP and tCNV could be calculated from raw data such as these, using the additive model, shown geometrically in Fig. 2. Each of the idealized CNVs shown at the bottom of Fig. 2 is the sum of an EAP, which is negative for downward and positive for upward eye rotations, plus a negative tCNV that precedes the ocular response to $9. The tCNVs are assumed to be identical for rotations made in either direction. The tCNV amplitude can be calculated simply by adding the pair of CNVs recorded during upward and downward rotations of equal extent; the EAPs cancel out and the sum represents twice the tCNV amplitude. Conversely, subtraction of the "downward" CNV from the "upward" one eliminates the tCNVs, leaving twice the EAP as the remainder. The subject of Fig. 1, V~ikeseveral others, exhibited vertical EOG deflections that were 2030% larger (absolutely) during downward eye movements than during upward ones. This disparity was tentatively attributed to differences in the extents of upward and downward rotationsL Such disparities would engender different-sized x The factors responsible for this commonly observed disparity of 20--30~ between EOG deflectionduring up. ward versus downward voluntary rotations were not identified with certitude. The most likely explanation is that subjects made systematicerrors of fixation,such that angular displacementsmade during the downward movements were absolutely larger; this could have resulted from the dots not beingexactly at the levelof the resting eye. However, a unidirectional shifting of the EOG electrodes in relation to the eye could have produced the ~me discrepancy. In the latter case, however,the EOG would not have borne a one-to-one relation with eyeball position relative to the skull, whichdeterminesthe EAP, and, therefore, the EAP-EOG functions would have been inaccurate. To rule out such an error, independent evidencewas presented for four subjects (Fig. 8) to show that the regressionfunc*.ions had made accurateand valid partitions. In the remaining subjects, however, their accuracy was not directlyverified; such would depend both upon the invarianceof the relation between the EOG and eye position, and the constancy of the tCNV during upward and downward rotations. Electroencep~. olin, NeitrophysioL, 1970, 28:173-182
! 76
S. A. HILLYARD AND R. GALAMBOS
EAPs, and this was accounted for by linear interpolations in the calculations, a sample of which foiiows: Using the data portrayed in Fig. I, the mean amplitude of EAP in the Cz channel is given by:
Throe
=.
EAP = [11.6 - - ( - 29.1)1/2= 20.4 pV
v
EAP = [19.6 - - ( - 34.0)]/2 = 26.8 pV in conjunction with a mean EOG deflection during these rotations of: EOG deflection- [138 - - ( - 175)]/2= 157 pV Such concurrent pairs of EAPs and EOG deflections produced at the different angles of dot separation are plotted for four subjects in Fig. 3. These EAP-EOG functions are graphed in terms of absolute amplitudes, because they apply to EAPs generated by either upward or downward eye movements. The growth of EAP with increasing EOG deflection was linear in all subjects, and the leastsquares method was used to obtain the lines of best fit. The strength of the linear relation is indicated by the statistic r 2, the square of the productmoment correlation. The parameters of the reII0
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[POTENTIAL SHIFT IN EOO] (pV) Fig. 3 Linear increase of eye movement artifact (EAP) in Cs (open circles) and frontal (solid circles) channels with increasing EOG deflections, all simultaneously induced by voluntary eye rotation. Absolute values indicate that the EAP and EOG deflection may be of either polarity. The least-squares regression lines and their slopes (b) and inter. cepts (a) for the C,, channel are given for each of the four subjects.
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gression lines did not differ significantly amo,g subjects. The rate of increase of EAP in the frontal channel was significantly steeper than in the Cz channel. Presumably, more artifact was induced in the frontal electrode per unit increment in the ocular field shift because this site was closer to the eyes. These EAP-EOG relationships were found to be invariant with large changes in initial eye position, thus ensuring their applicability to the Si-S~-respond condition, wherein initial eye position was not controlled. tCNV preceding voluntary eye movemenl~, The mean tCNV during the 0.3 sec before S~ ranged between - 0 . 4 and -21.3 pV, with an over-all mean of - 5.9 pV on all trials enacted under "low effort" conditions. Analysis of variance showed that there was no effect of the size of eye move. ment upon the amplitude of the tCNV. The tCNV was greatly augmented when the ocular response to Ss was made with"high effort" (rapid response) in three subjects. The m~an tCNV was incremented from - 4 . 8 ~V, for low effort rotations of l0 °, to - 16+0pV, a highly significant increase (F(l,9)-- 15.81,P < 0.01) (Fig. 4). Although increasing the speed of the return response greatly enhanced the tCNV, the EAP produced by these l0 ° displacements remained Eiectroenceph. clin. Neurophysiol., 1970, 2.8:173-182
177
EYE MOVEMENTS AND CNV
unchanged. The tCNV could thus be increased independently from the EAP, whereas the EAP could be independently enlarged by making bigger eye movements. This demonstrates the existence of two additive, separable components in the CNV, one determined by response effort and the other by ocular displacement.
Synchronized with the CNV was a consistent potential shift in the EOG, reflecting a pattern of involuntary eye movement. Fig. 5 shows typical CNVs and simultaneously rvcorded EOGs from nine subjects. The most common EOG wave form was a large negative shift (downward eye rotation) that peaked near the onset of Ss and bore a disturbing resemblance to the scalp-recorded CNV. In other subjects, however, the EOG deflections were very small, or even positive for part of the St-Ss interval. Lateral eye movements, as indexed by the horizontal EOG, were invariably too small to contribute artifact to the scalp channels and will not be considered further. Although each subject exhibited an idiosyncratic pattern of eye movements, there was substantial trial-to-trial variation in the quantified magnitude of the EOG deflection, which introduced considerable variability into the CNV. Using each individual's regression function (as in Fig. 3), the averaged CNVs were algebraically segregated into EAP and tCNV components; the trial-to-trial variation of these potentials within two subjects is shown in Fig. 6. The right hand
Control trials When no motor responses were made, the potential shift in the Cz channel within the 0.3 sec preceding Ss was within noise levels, averaging - 0 . 5 pV over all subjects on the 16 trials. The mean deflection in the EOG was also negligible. Si-S~-respond trials When lever presses were made at the onset of Ss, large CNVs developed in both C,~ and frontal channels within the first few trials. Each subject displayed a distinctive CNV wave form that was recognizable from one block of trials to the next, but varied considerably in amplitude. The mean CNV (Cz channel) from all trials ranged between - 16.2 and - 38.6/tV in different subjects.
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178
S.A. HILLYARD AND R. GALAMBO$
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Fig. 6 Spontaneous variation in the CNV and its two components, EAP and tCNV (vertically hatched area), averaged over successive blocks of eight trials with the eye~ closed in two subjects. The number assigned to each block is the percentage of the CNV that was constituted by EAP on those trials.
column of Table l gives the range of EAPs exhibited by each subject on different blocks of trial~, In the five subjects with large EAPs (aver. aging more than 25°/,, of the CNV), there was a higher correlation of EAP with CNV amplitude (average Pearson r=0.72) than of tCNV with CNV amplitude (average r=0.31). This means that the ocular artifact could contribute more to the variance of the CNV than did the "cerebral" component. In general, tCNV amplitudes were independent of the size of the EAP, even in subjects making large eye movements. The mean amplitudes over all trials of CNV, EAP and tCN~', in C~ and frontal channels, and the mean per cent EAP/CNV are presented in Table [ for each subject. On the average across all subj~ts, -6.4 pV or 23% of the CNV was corn. posed of artifact, resulting from a net tendency to move the eyes downward during the $1-58 interval when the eyes were closed.
Validity of the partition of CNV. CNVs from three subjects were computer-averaged in blocks of 12, grouped together on the basis of the size of the EOG deflections. This procedure produced pairs of averaged responses like those in Fig. 7, making conspicuous the dependence of CNV upon the EOG deflection. The growth of CNV with increased EOG deflection confirms that the latter potential shift was actually caused by an ocular rotation that engendered an electric field at the scalp, rather than by movement of the EOG electrodes or some other localized process. Furthermore, this dependence of CNV upon the EOG deflection was linear, with a slope that was usually identical to that of the EAP-EOG function. The final demonstration of the validity of dividing the CNV into tCNV and EAP components is based upon data obtained from four subjects, during S1-S~-respond trials enacted with the eyes fixed on a target. Representative CNVs and concomitant EOGs from these subjects are shown in Fig. 8. In each case a substantial CNV was evident in the absence of any ocular deviation, and, therefore, consisted of tCNV. The mean tCNV from these subjects, measured over 200 eyes-fixated trials, was - 21.4pV in the Czchannel. The mean tCNV calculated from 250 separate eyes-closed trials in the same subjects was -22.9 pV. In the frontal channel, the mean tCNV was -13.0/~V on eyes-fixated trials and was calculated to be -13.4 pV on eyes-closed trials. The correspondence between these magnitudes demonstrates the accuracy of the partition of CNV by the regression function. DISCUSSION
A significant proportion of the CNV in most subjects was comprised of electric fields spreading passively from the corneo-retinal dipole, which was rut~ted involuntarily during leverpressing trials when the eyes were closed. On the average, across all subjects, -6.4/~V or 230/0 of the CNV was composed of artifact, but the EAP often reached - 10 to - 20/~V, due to systematic, downward eye rotations synchronized to the task. In fact, in those subjects whose eye movements were large, the EAP contributed more to the variance of the CNV than did the "cerebral" component. Electroenceph. din. Neurophysiol., 1970, 28:173-182
179
EYE MOVEMENTS AND CNV
B
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Fig. 7 Dependency of CNV amplitude upon the magnitude of the concurrent E O G deflection in two subjects. Tracings are computer averages from 12 trials selected for having large negative (A), intermediate (/3), and large positive (C) EOG deflections. Calibrations: CNV = 20/tV; E@G = 100/~V.
TABLE 1 Mean amplitude of CNV and its components (in/~V) for each subject during St-Sa-respond trials with eyes closed CNV
EAP
tCNV
EAP/CNV (per cent)
Range of EAP amplitudes*
EIO MeG COL CQK WOW LZO WRG GUS FOU CLY
--25.3 -29.7 --37.5 -38.6 -28.4 --29.5 -- 16.2 --25.1 --23.4 --18.8
- 6.9 + 2.9 -12.7 - 5.8 - 10.8 - 1.7 -- 1.4 -- 4.2 --17.8 -- 5.6
- 18.4 -32.6 -24.8 -32.8 - 17.6 -27.8 -- 14.8 --20.9 -- 5.6 --13.2
27 -10 33 15 38 6 9 t7 76 30
+ 6,0, - 18.0 + 1 0 . 5 , - - 6.3 -- 5 . 0 , - 3 9 . 8 0 ,9.5 - 0.8, - 2 0 . 5 -- 0 . 6 , - 2.5 + 0.9, -- 5.0 -- 1 . 6 , - 5.6 --12.0,--24.9 -- 0 . 1 , - - 1 0 . 6
Mean
--27.3
-- 6.4
--20.9
23
-- 8.0 -- 16.0 -- 3.9 -- 9.3
-- 16.2 -- 10.5 -- 19.9 --15.5
33 60 16 36
Subject
Cmchannel
Frontal channel EIO WOW LZO Mean
--24.2 --26.5 --23.8 --24.8
+ 6.3,-23.9 -- 2 . 2 , - 2 8 . 1 - 1.8,6.1
* These are maximum negative and positive EAPs that were observed when responses were averaged in blocks of eight sequential trials.
Electroenceplt. clin. Neurophyslol., 19'/0, 28:173-182
180
S.A. HILLYARD A N D R. G A L A M B O S
~
LZO
s.t
¢NV--EOG-
CNV--~ I Fig. 8 CNVs recorded from Cz channel and the concurrent EOGs from four subjects, averaged ovvr one block of S1-S~-respond trials while the eyes were fixated upon a central target. Large positive waves in the EOG were caused by eye-blinks following S~. Calibrations: CNV = 20pV; EOG = 100pV.
In some of the earlier studies cited above, correlations were observed between small changes in CNV amplitude (of 5-10 pV) and various stimulus and behavioral variables. In many cases such •/ariation could have resulted from changes in eye movement patterns instead of changes in a brain potential. If the size of eye movements happened to covary with a particular behavioral variable, an oculomotor-behavioral relationship might be misinterpreted as an electrocerebral-behavioral one. Most of the more recent investigations, however, have displayed an awareness of the ocular contamination problem and have controlled for it with more or less rigor by one of the techniques described below. The simplest and most reliable way to isolate the tCNV from ocular potentials was found to be .~.recording with the eyes fixated on a point, which generally eliminated slow eye movements. A more complicated but equally valid technique was the estimation of EAP magnitudes by concurrent recording of the calibrated vertical EOG. Walter (1967) has described a third method for attenu. ating this artifact from scalp recordings; the reference lead was attached to a potentiometer, which balanced the resistance between a linked mastoid and a supra-orbital electrode, so that EAPs induced at the vertex and at the virtual reference were equal. The validity of this method would seem to depend upon a linear relation between potential shifts in the reference lead andEAPs at the vertex, which is substantiated by the iinearity of the present EAP-EOG functions. A
final method, indirect though acceptable if carefully quantified, was to show that eye movements are equal in size under different experimental conditions (Tecce and Scheff 1969). The distribution of potential shifts induced across the scalp by eye movements and blinks has been plotted previously (Zao et al. 1952; Peters 1967), but not for displacements of much less than 10°, which demands the use of computer averaging techniques and segregation of the con. founding tCNVs. Rowland (1968), however, has cited reports that "small" voluntary movements can cause DC artifacts that decline in amplitude with distance from the eye, but are clearly present even at the oc~iput; he also reported that in half of the subjects, CNV recordings were severely contaminated by such artifact, even during attempted visual fixation. Cant et aL (1966) also discovered that eye movements must be excluded before DC shl~'ts of cerebral origin could be assessed, particularly when complex visual stimuli were used. These findings suggest that the later components of scalp evoked potentials could also suffer ocular contamination if an eye blink or "twitch" was evoked by the stimulus. Goffet al. (1969) have identified such artifacts in the evoked potentials on the human scalp, but found their spatial distributions limited to frontal regions. Nonetheless, it is possible that certain individuals or manipulations (Rietveld 1966) may produce large, phasic eye displacements which would influence more posterior recording sites. Electroenceph. clin. Neurophysiol., 1970, 28:173-182
EYE M O V E M E N T S A N D C N V
The tCNV was found to be independent from the EAP in both lever-pressing and voluntary eye-moving tasks. The tCNV preceding voluntary eye movement was enhanced by increasing response speed and effort, while in thelever-pressing task the tCNV was often correlated with reaction time (Hillyard 1969a). The correspondence of the tCNV with such response dimensions supports the thesis that it is a response-governirtg brain potential, associated with the psychological constructs of preparatory set, response selection (Donald 1968) and conation (Low et al. 1966). SUMMARY
During the preparatory interval between a warning click and a tone burst that signalled a lever press, a slow negative potential shift (CNV) was recorded from the scalp in ten normal adults. When the eyes were closed, involuntary eye movements during the click-tone interval consistently generated potential shifts which spread from the corneo-retinal dipole to the scalp electrodes and thereby contaminated the CNV. The CNV was quantitatively partitioned into an artifactual component caused by ocular rotation (the EAI ), which summated with the second component, presumably of cerebral origin, called the "true" or tCNV. The EAP amplitudes were estimated from concurrent recordings of the electro-oculogram. In the average subject, 23% or -6.1/~V of the total CNV was comprised of EAP, and the EAP often reached from - 1 0 to - 1 5 /~V. The accuracy of the partition was verified by comparing tCNVs recorded with eyes closed and with eyes immobilized by fixation. The CNV produced during voluntary eye movements was similarly divided into a tCNV, which was tripled in amplitude when ocular responses were made with increased speed and effort, and an EAP, which was determined solely by the amount of ocular displacement.
R~SUM~ ART~,FACTDO AUX MOUVEMENTSDES YEUX DANS LA VARIATION CONTINGENTE NI~GATIVE
Au cours de l'intervalle pr6paratoire entre un clic d'avertissement et une s~rie de sons qui constitue le signal de presser un levier, un potentiel n~gatif lent (VCN) est enr©gistr~ au niveau de
181
scalp chez dix adultes normaux. Lorsque les yeux sont ferm6s, des mouvements involontaires des yeux darts l'intervalle entre le clic et les bruits produisent de fro;on constante des variations de potentiel qui diffusent du dipole corn6o-r6tinien attx ~lectrodes de scalp et ainsi contaminent la VCN. La VCN se r6partit quantitativement en une composante artffactielle caus6e par la rotation oculaire, qai s'additionne ~tla seconde composante probablement d'origine c~r6brale, appel6e la v6ritable variation contingente n6gative (VVCN). Les amplitudes de la composante artffactielle peuvent 8tre appr6ci6.es /i partir d'enregistrements simultan6s d'61ectro-oculogrammes. En moyenne, 23% ou -6.1 /~V de la VCN totale consiste en potentiels artffactiels qui atteignent souvent de - 10/t - 15/IV. La pr~ision de cette r6partition est v6rifi6e en comparant les vraies variations contingentes n6gatives enregistr~es les yeux ferm~s et les yeux immobilis6s par fixation. La VCN provoqu6e pendant les mouvements oculaires vo~ontaires sont de meme divis6s en une vraie variation contingente n6gative, qui est tripl6e en amplitude quand les r6ponses oculaires se font avec une vitesse et un effort accrus, et une composante artffactielle qui n'est due qu'~ ia quantit6 de d~placement oculaire. ,,
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