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ERP response decrement and recovery as a function of stimulus type and scalp location
Physiology &Behavtor, Vol. 19, pp. 15-22. Pergamon Press and Brain Research Publ, 1977. Printed m the U.S.A.
ERP Response Decrement and Recovery as a Function of Stimulus Type and Scalp Locatioff A N D R E A L. M E G E L A 2, T I M O T H Y J. T E Y L E R 3 A N D G A R Y W. H E S S E
Department o f Psychology and Social Relations, Harvard University, Cambridge, MA 02138 (Received 10 D e c e m b e r 1976) MEGELA, A. L., T. J. TEYLER AND G. W. HESSE. ERP response decrement and recovery as a functlon of sttmulus type and scalp location PHYSIOL. BEHAV. 19(1) 15-22, 1977. - - Response decrement and recovery of visual event-related potentials (ERPs) at different electrode sites to different types of repetitive stimuli were studied. Nine blocks of stimuli were presented in the form AAAAAABB. Stimuli were of four types: diffuse flashes of light, geometric shapes, words of similar meanings, and words of dissimilar meanings. The relative amounts of ERP response decrement and recovery differed as a function of ERP response components measured (early vs. late), electrode site (left frontal, left temporoparietal, and left occipital), and stimulus type. Early components were sensitive to sensory characteristics of the stimuli. Late components from the left temporoparletal site were sensitive to the meanings of the linguistic stimuh. The research suggests a useful paradigm for the study of habituation-like responses and of cerebral specificity in an intact normal population. Event-related potentials Intensity generalization
Visual evoked potentials Habituation
Response decrement
WE H A V E e m p l o y e d a h a b i t u a t l o n / g e n e r a h z a t i o n paradigm in an a t t e m p t to examine differences in l n t r a h e m l s p h e n c event-related potentials (ERPs) to several classes of hngulstlc and n o n h n g m s t l c stimuli. R e c e n t l y , it has been d e m o n s t r a t e d that ERPs recorded from the h u m a n scalp exhibit several of the parametric features of h a b i t u a t i o n as defined by T h o m p s o n and Spencer [ 2 5 ] . These include a m p h t u d e d e c r e m e n t s following a negative e x p o n e n t i a l f u n c t i o n ; s p o n t a n e o u s recovery, the direct relation b e t w e e n stimulus f r e q u e n c y and degree o f h a b i t u a t i o n , the inverse relation b e t w e e n stimulus intensity and degree of habituation, and stimulus generahzatlon [1, 2, 3, 4, 7, 8, 12, 14, 15, 16, 18, 2 0 ] . All of the parametric features of h a b i t u a t i o n have not, however, been observed m the ERP, suggesting caution m interpreting these results as an instance of habituation. Since the ERPs in the present study are n o t e x a m i n e d for all of the parametric features of habituation, we shall e m p l o y the m o r e conservatwe term response d e c r e m e n t The d e m o n s t r a t i o n that ERPs exhibit response dec r e m e n t and recovery m a h a b i t u a t i o n / g e n e r a l i z a t i o n paradigm is of interest for several reasons. First of all, differing theoretical predictions concerning the nature of h a b i t u a t i o n [9, 21, 25] could be tested with this paradigm. F u r t h e r m o r e , by recording ERPs from several different scalp locations, cerebral locahzat~on and f u n c t i o n in an
Cerebral specificity
intact normal population could be investigated, with a m e t h o d wh,ch c o m p l e m e n t s and extends previous research based on behavioral measures (e g., [ 5 ] ). The procedure used m this study revolved the rapid presentatxon of a series of identical stxmuh followed by a test stimulus differing on one or m o r e dimensions. The ERP response to the repeated identical stimuli (the h a b i t u a t i o n stimuh) was e x p e c t e d to decrement. The degree to which ERPs to the h a b i t u a t i o n and test (generahzatlon) stlmuh were related reflected the underlying cerebral processing of the two stimulus types If the a m p h t u d e of the ERP to the generahzatlon stimulus was equal to or smaller than the amplitude of the ERP to the last habltuat~on stimulus of the series (e.g., the response remained d e c r e m e n t e d ) , we assumed that the two stlmuh were being processed similarly. Conversely, xf the response to the generahzatlon stimulus was larger than that to the last habituataon stimulus of the series (e g., the response recovered), we assumed that the two stimuli were being processed differently. The relative a m o u n t s of response change represent an index of the degree to which a specific cortical site is processing the difference b e t w e e n the stlmuh. F o r example, a similar response to two different stlmuh indicates that the dimension across which the stimuli differ is n o t being processed at that s~te. We hypothesized that the relative a m o u n t s of ERP
1Supported by an N.I.M.H predoctoral fellowship and a grant from the Department of Psychology and Social Relations, Harvard University, to the first author, and a grant from the Milton Fund of Harvard Umversity to the second author. We thank P Clark, R. H. Dworkln, R, Hastie and L. Teyler for their valuable assistance. 2Now at the Section of Neurobiology and Behavior, Largmutr Laboratory, Comell University, Ithaca, New York 14853 Send reprint requests to this address. 3 Now at the Neurobtology Program, Northeastern Ohio Universities College of Medicine, Rootstown, Ohio 44272. 15
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r e s p o n s e d e c r e m e n t and r e c o v e r y would differ as a t u n c t l o n of e l e c t r o d e scalp l o c a t i o n (left f r o n t a l , left telnporoparaetal or left occipital), s t i m u l u s t y p e (linguistic or n o n h n g u l s t l c ) , a n d the specific E R P c o m p o n e n t m e a s u r e d {early or l a t e ) We p r e d i c t e d t h a t early c o m p o n e n t s , o c c u r r i n g b e t w e e n 50 a n d 250 msec p o s t s t i m u l u s o n s e t , w o u l d process the sensory aspects o f b o t h linguistic and n o n h n g u i s t l c s t i m u h , especially at the o c c i p i t a l l o c a t i o n , in a c c o r d w i t h p r e v i o u s w o r k o n visual e v o k e d p o t e n t i a l s [ 1 7 ] . Late c o m p o n e n t s , o c c u r r i n g b e t w e e n 2 5 0 a n d 4 0 0 msec p o s t s t l m u l u s o n s e t , were e x p e c t e d to be less sensitive to the sensory aspects and m o r e sensitive to the s e m a n t i c aspects of t h e h n g u l s t l c stimuli, since these c o m p o n e n t s are b e i n g r e c o r d e d f r o m t h e left h e m i s p h e r e and have b e e n s h o w n to be sensitive to cognitive and h n g u l s t l c variables [ 11, 19, 221 F o r e x a m p l e , w i t h a pair of linguistic stimuli of Identical m e a n i n g s b u t d i f f e r e n t physical characteristics, t h e occipital early c o m p o n e n t s w o u l d be e x p e c t e d to show r e s p o n s e r e c o v e r y because o f the physical d i f f e r e n c e s b e t w e e n the stimuli The t e m p o r o p a r a e t a l late c o m p o n e n t responses, p r e s u m a b l y reflecting activity f r o m areas of the left h e m i s p h e r e i m p o r t a n t for language r e c e p t i o n [ 1 3 ] , would r e m a i n d e c r e m e n t e d to these t w o s t i m u h o f i d e n t i c a l m e a n i n g . On t h e o t h e r h a n d , for n o n h n g u l s t l c stimuli of d i f f e r e n t physical characteristics, occipital, t e m p o r o p a r l e t a l a n d f r o n t a l early c o m p o n e n t s w o u l d all be e x p e c t e d to show r e c o v e r y of r e s p o n s e to the g e n e r a h z a t l o n s t i m u l u s if early c o m p o n e n t left h e m i s p h e r e ERPs e n c o d e o n l y physical aspects of nonlanguastlc stlmUh Late c o m p o n e n t E R P r e s p o n s e s w o u l d n o t be e x p e c t e d to show recovery to nonhnguastac g e n e r a h z a t I o n stimuli if these r e s p o n s e s are n o t sensitive to n o n h n g u l s t l c stimuli METHOD
T h r e e m a l e s a n d seven females, aged 19 33 years, p a r t i c i p a t e d in t h e e x p e r i m e n t All were r i g h t - h a n d e d , w i t h n o f a m i l y h i s t o r y of l e f t - h a n d e d n e s s . E a c h subject part l c i p a t e d in a single e x p e r i m e n t a l sessmn lasting a p p r o x i m a t e l y t w o hr. E E G was r e c o r d e d f r o m t h r e e scalp l o c a t i o n s F3, 01, and a t e m p o r o p a r i e t a l p l a c e m e n t equid i s t a n t b e t w e e n C3, T3 a n d P3 ( I n t e r n a t i o n a l 1 0 - 2 0 system, [ 1 0 1 ) E l e c t r o d e s were m i n i a t u r e B e c k m a n silversilver c h l o r i d e , held in place b y a s t r e t c h a b l e lycra cap w o r n b y the subjects. L i n k e d ears served as r e f e r e n c e , a n d a f o r e a r m e l e c t r o d e served as g r o u n d Eye m o v e m e n t s were r e c o r d e d f r o m e l e c t r o d e s p l a c e d lateral to and u n d e r n e a t h the right eye. All e l e c t r o d e resistances were k e p t b e l o w 10 k a E E G a n d E O G activity were a m p l i f i e d t h r o u g h a Grass M o d e l 7 p o l y g r a p h ( b a n d p a s s 1 - 3 5 c/sec) and r e c o r d e d o n FM tape for off-line analysis by a PDP-9 c o m p u t e r . E E G was averaged at a s a m p l i n g rate o f 512 c/sec for 5 0 0 msec e p o c h s b e g i n n i n g w i t h s t i m u l u s onset. Stimuli were p r e s e n t e d b y t w o slide p r o j e c t o r s e q u i p p e d w i t h G e r b r a n d s t a c h l s t o s c o p l c s h u t t e r s activated b y Massey-Dickinson programming equipment To avoid a u d i t o r y c o n t a m i n a t i o n o f the visual ERPs, the noise o f the s h u t t e r s was m a s k e d b y b a c k g r o u n d w h i t e noise Simu l t a n e o u s w i t h s h u t t e r o p e n i n g , a 2 V, 5 0 0 msec pulse also a c t i v a t e d by the p r o g r a m m i n g e q u i p m e n t was placed o n tape a n d s u b s e q u e n t l y used to trigger t h e c o m p u t e r for E R P averaging. S t l m u h were b a c k - p r o j e c t e d o n t o a screen in a s o u n d - d e a d e n i n g r e c o r d i n g c h a m b e r in w h i c h s u b j e c t s were seated
The e x p e r i m e n t a l s e s s I o n consisted t~l t l l r l t ~ S C p d [ a { ~ b l o c k s of s t l m u h Each b l o c k was c o m p o s e d of t w o s t m l u : J , A and B, p r e s e n t e d in the s e q u e n c e A A A A & a , BB S1Hnulu~ A was the h a b i t u a t i o n stimulus, s t i m u l u s B was ~tle g e n e r a l i z a t i o n s t i m u l u s Within each block, average~ ~ e r c m a d e t r o m the h r s t 10 artifact-free stmmlu~ wquetices, w i t h a m a x i m u m of 15 s e q u e n c e s being p r e s e n t e d pel b l o c k This relatively small n u m b e r of s t i m u l u s r e p e t i t i o n s was c h o s e n to lessen the total time ol the e x p e N m e n t a t session m o r d e r to avoid subject fatigue and any pOsblble s t i m u l u s satiat~on effects W~thln each s t u n u l u s s e q u e m e , the l n t e r s t i m u l u s lnterx.al was 1600 msec t'ach 800 nlsec d u r a t m n s t i m u l u s being p r e c e d e d by an 800 msec i i x a t l o n p o i n t T h e interval b e t w e e n s t i m u l u s s e q u e n c e s w i t h i n a b l o c k varied b e t w e e n 10 and 12 sec, while the lntelval b e t w e e n b l o c k s was a p p r o x i m a t e l y 5 m m Fhe order ol s t i m u l u s blocks was r a n d o m l z e d for each sublect S u b j e c t s were n o t r e q u i r e d to r e s p o n d to the s t l m u h T h e y were i n s t r u c t e d , h o w e v e r , to avoid gross bodily m o v e l n e n t s and e y e b h n k s a n d to m a i n t a i n tLxation during p r e s e n t a t i o n ol stimuli P o l y g r a p h records weie e x a m i n e d lor these sources of c o n t a m i n a t i o n and the trials e h m i n a l e d from the average The relatively sho~t time span ot each stimulus b l o c k h e l p e d to ensure t h a t subjects r e m a i n e d a(tenll~e d u r i n g each b l o c k The nine d i f f e r e n t s t i m u l u s pairs r e p r e s e n t e d three classes n o n h n g u l s t l c s t l m u h (5 pair), linguistic stimuli of similar or identical m e a n i n g s (3 pair), and hngulstlc s t m l u h of d i f f e r e n t m e a n i n g s b u t slinllar physical c h a r a c t e r i s t i c s l 1 pair) The n o n h n g u l s t l C stimuli were h n e drawlng~ ot varying c o m p l e x l t } t h a t were n o t easily e n c o d e d verbally and diffuse flashes of light Linguistic stltnuh ot smlflar m e a n i n g s were s y n o n y m s , linguistic s t i m u h oI identical m e a n i n g s consisted ol the same word p r e s e n t e d in d i f f e r e n t t y p e f o n t s Linguistic s t l m u h of d i f f e r e n t m e a n i n g s were c h o s e n to be very sm~ilar along every d i m e n s i o n e x c e p t s e m a n t i c E x c e p t for the diffuse flashes ot light, l u m i n a n c e level was e q u a t e d w i t h i n each pair of SlllnUll The nine d i f f e r e n t s t i m u l u s pairs are s h o w n in Table 1 4 s ~an be seen from this table, in one s t i m u l u s block ( n o n l l n g u l s t l c geometrlc}, no generalization stimulus appeared In a d d i t i o n , t w o n o n h n g u l s t l c blocks were c o m p o s e d o1 the same pmr of stimuli b u t p r e s e n t e d in d i f f e r e n t positions, 1.e, A A A A A A B B and B B B B B B A A f o r m e d the two diff e r e n t blocks This was also true of t w o llngmstlc b l o c k s Within each s t i m u l u s block, average 1~RPs were c o m p u t e d across s t n n u l u s s e q u e n c e s for stimuli nl p o s i t i o n n u m b e r s 1, 4, 6, and 7 t t h e first g e n e r a l t z a t m n .~tmmlus} This p r o d u c e d a s t i m u l u s - b y - s t i m u l u s average consisting of all initial stamuh w i t h i n a p a r t i c u l a r block, all f o u r t h stimuli, etc, (see [ 1 8 ] ) After averaging, the ERPs were p h o t o g r a p h e d f r o m a c o m p u t e r slave screen These p h o t o graphs were enlarged and m e a s u r e d to o b t a i n c o m p o n e n t a m p l i t u d e s All a m p l i t u d e m e a s u r e m e n t s were m a d e in a b l i n d m a n n e r , the scorer b e i n g u n a w a r e uf s t i m u l u s type, e l e c t r o d e l o c a t i o n or s t i m u l u s p o s i t i o n for any ot the ERPs F o r each ERP, two c o m p o n e n t s were m e a s u r e d peakt o - p e a k a m p l i t u d e s of N, P~, defined as the largest negative-positive d e f l e c t m n in the latency ~ange 5 0 - 2 5 0 msec, a n d b a s e h n e - t o - p e a k a m p l i t u d e of P3, defined as the largest positive d e f l e c t i o n relative to baseline in the latency range 250 4 0 0 msec These relatively b r o a d l a t e n c y ranges were c h o s e n because of the great i n t e r and lntraindavidual variability e x p e c t e d in the ERPs across t h e d i f f e r e n t s t l m u h used A c t u a l r e s p o n s e latencies of c o m p o n e n t peaks within
ERP RESPONSE DECREMENT
17
each temporal window were substantially less broad; the values are reported below. For each stimulus pair, early and late c o m p o n e n t amplitudes were separately analyzed by a two-way repeated measures analysis of variance (ANOVA) [6,29] with electrode sites and stimulus position as the repeated measures. Eighteen separate ANOVAs were computed. For each ANOVA, five F-tests were computed - main effects for site and for position, hnear and quadratic trends for position, and the site by position interaction. Linear and quadratic trend analyses were performed in order to assess the profile of amplitude change across stimulus position. In this design, a linear trend implies a consistent decrease in amplitude across stimulus position, while a quadratic trend implies a decrease followed by recovery [29]. Although all nine stimulus blocks were presented to each subject, eyebhnks, eye movement, or muscle artifacts forced ehm1nation of at least one block for 8 of the 10 subjects The different number of subjects for each ANOVA and the analyses for trend components are reflected in the different degrees of freedom for the F-ratios (degrees of freedom are reported along with F values) RESULTS
Nonhngutstlc Sttmu h Sample ERP waveforms superimposed~ for all subjects from one pair of nonhnguistlc stimuli are presented m Fig 1 Mean percentage changes in amplitude of early and
FRONTAL
late components for three pairs of nonlinguistlc stimuli are shown in Fig. 2 Two flashes of different brJghtnesses, counterbalanced for direction of brightness change, served as stimuli. For the dim/bright pair, the N 1 P2 components showed response decrement to the dim flash and response recovery to the bright flash as shown by a mare effect for position, F(3,27) = 5.01, p = 0.007, with a significant quadratic trend, F(1,9) = 2 1 . 3 2 ; p = 0.001 For the bright/dim flashes, the occipital responses recovered in response to the dim flash while the temporoparletal and frontal leads showed no significant response recovery, F(6,42) = 2 32; p = 0.05 Thus, when the generalization stimulus was brighter or dimmer than the habituation stimulus, occipital early components processed this difference, whale frontal and temporoparietal early components did so only In the case of the brighter generalization flash Late components for both pairs of flashes evidenced nonsignificant quadratic trends for position This suggests that P3 components from both anterior and posterior left hemisphere sites may not reliably process brightness differences between these nonllngulstlc stlmuh Early component ERPs at all sites to the simple line drawings decremented over stimulus positions 1 to 6, F(3,24) = 3.84; p = 0.02, and recovered in response to the generalization stimulus (quadratic trend, F ( 1 , 8 ) = 5.49, p < 0 05). A main effect for site, F(2,16) = 6 . 6 4 ; p = 0 008, indicated that a relatively greater amount of response decrement and more recovery occurred at the temporo-
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FIG 2. Mean percentage amplitude changes over all stimulus positions for three pairs of nonllngmstlc stimuli. Response at position l has been set to 100% Early (NIP~) and late (P3) component responses are presented separately Each data point represents the mean amplitude over all subjects Electrode sites are F, left frontal; T, left temporoparIetal, and O, left occipital
parietal lead P a t t e r n s of a m p h t u d e change for the P3 c o m p o n e n t were n o t s~gmflcant Early c o m p o n e n t r e s p o n s e s to t h e c o m p l e x g e o m e t r i c shapes s h o w e d a significant q u a d r a t i c t r e n d over s t i m u l u s p o s i t r o n , F ( 1 , 8 ) = 10.36, p = 0 01, and a m a r e effect for s~te, F ( 2 , 1 6 ) = 7 . 2 9 ; p = 0 006, w i t h little a m p h t u d e c h a n g e o c c u r r i n g at the t e m p o r o p a r l e t a l lead Late c o m p o n e n t r e s p o n s e s to this s h m u l u s pair, u n l i k e t h o s e to t h e o t h e r n o n h n g m s t l c pmrs, also e x h i b i t e d a s l g m f l c a n t m a r e e f f e c t for p o s i t r o n , F ( 3 , 2 4 ) = 3 16, p = 0 04, w i t h a s~gnlflcant quadratic trend, F(1,8)= 5 75, p = 0 0 4 , the f r o n t a l r e s p o n s e r e c o v e r i n g m o r e t h a n the o t h e r responses. Th~s suggests t h a t t h e f r o n t a l E R P s m a y have b e e n processing c o m p l e x i t y or n o v e l t y of the s h m u h , r a t h e r t h a n t h e i r n o n h n g u l s t l c n a t u r e per se Finally, a n o - c h a n g e c o n d i t i o n , in w h i c h the same simple h n e d r a w i n g a p p e a r e d m all m g h t s t i m u l u s p o s i t i o n s per s e q u e n c e , was i n c o r p o r a t e d in the design As p r e d i c t e d , a r o b u s t l i n e a r e f f e c t for positron, md~catlng c o n t i n u e d d e c r e m e n t o f r e s p o n s e for all 8 s t i m u l u s p o s m o n s , o c c u r r e d for early c o m p o n e n t s , F ( 1 , 6 ) = 4 0 6 6 , p = 0 001 A m a i n e f f e c t of s~te, F ( 2 , 1 2 ) = 7 3 9 , p = 0 0 0 8 , suggested t h a t the
S a m p l e ERP w a v e f o r m s l r o m all subjects for one pair ol linguistic s t l m u h are p r e s e n t e d in Fig 3 Mean p e r c e n t a g e changes m a m p l i t u d e of early and late c o m p o n e n t s toJ t h r e e pairs ot linguistic s t l m u h are p r e s e n t e d in F~g 4 Early a n d late c o m p o n e n t ~ e x h i b i t e d d i f f e r e n t p a t t e r n s of a m p l i t u d e change in response to the hnguistlc stamuh N 1 P: a m p l i t u d e s to the s h m u l u s pmr identical m m e a n i n g b u t differing in physical c h a r a c t e n s h c s ( d o g / D O G ) s h o w e d a s]gnlflcant mare effect ol pos]tion, F ( 3 , 2 4 ) = 3 3 8 , p = 0 0 3 , with a q u a d r a t i c t r e n d , F ( 1 , 8 ) = 5 5b, p < 0 0 5 . m d l c a t l n g r e s p o n s e d e c r e m e n t over p o s i U o n s 1 to 0, wiltl recovery o c c u r r i n g to the g e n e r a h z a t i o n s t i m u l u s Thus, all e l e c t r o d e sites were r e s p o n s w e to the ph~cslcal dJlferenee~ b e t w e e n these t w o s h m u h A o n e - t a f l e d t - t e s t t o r c o r r e l a t e d m e a n s [29] i n d i c a t e d t h a t significantly greater recover3 ol r e s p o n s e o c c u r r e d at occipital t h a n at frontal or t e m p o r o parietal sites, t ( 8 ) = 3 08. p . 0 0 1 P3 a m p h t u d e s from t e m p o r o p a r i e t a l and f r o n t a l sites to this s t i m u l u s pair. w h d e again d e c r e m e n t i n g over p o s i t i o n s 1 to 6, did n o t ~ignfflcantly recover In response to the g e n e r a l i z a t i o n q~rnulus The m a i n e t l e c t f o r p o s m o n , F ( 3 , 2 4 ) = 3 8 7 , / 9 = 0 0 2 , a p p e a r e d with only a marginally significant linear t r e n d , F(1,8) = 464, p = 00b T-tests s h o w e d a s l g m h c a n t increase in r e s p o n s e to the g e n e r a l i z a t i o n ~txmulus at the occipital lead, t ( 8 ) = 1 95, p 0 0 5 , w i t h t e m p o r o p a n c l a I and f r o n t a l leads e x h i b i t i n g httle r e c o v e r y to that stlmulu.~ This suggests t h a t , as with several of the n o n l l n g m s t l e s t l m u h , P3 c o m p o n e n t s did n o t reliably process physical differences, h o w e v e r , as p r e d i c t e d , P3 c o m p o n e n t s lronl ~rontal a n d t e m p o r o p a r l e t a l sites were ~cns~t~ve to the s e m a n h c f e a t u r e s ol these ~timuh S e m a n t i c elfe~ts were l u r t h e r investigated w~th the s y n o n y m pairs ol Stllnuh l n t e r p r e t a t m n of these Jesuits, h o w e v e r , m u s t be viewed with c a u t i o n , as the t r e n d s o b s e r v e d were n o t s y m m e t r i c a l b e t w e e n the two pmrs F o r one pair ( J U M P / L E A P ) , early c o m p o n e n t s significantly c h a n g e d over s h m u l u s posit]on, F ( 3 , 2 1 ) = 3 0 7 , / 9 = 0 05 with a q u a d r a t i c t r e n d a c c o u n t i n g for the effect at all e l e c t r o d e sites F o r the reverse pair (LEAP~JUMP), this result held true for the occipital and t e m p o r o p a r i e t a l s~tes only, as s h o w n by a m a i n effect for site, F ( 2 , 1 6 ) = 4 4 2 , p = 0 03 T h u s , m general, early c o m p o n e n t s were n o t ~cns]tlve to the s e m a n t i c similarity b e t w e e n these s t l m u h As p r e d i c t e d , P3 c o m p o n e n t s to one s y n o n y m pair ( J U M P / L E A P ) e v i d e n c e d a r o b u s t h n e a r effect over stimulus p o s i t i o n , F ( I , 7 ) = 10.76, p = 0.01, all ot the lead~ s h o w i n g h t t l e r e s p o n s e recovery to s h m u l u s 7 F o r the reverse s y n o n y m pair, a marginally slgmflcant site by p o s i t r o n i n t e r a c t i o n a p p e a r e d , F ( 6 , 4 8 ) = 2 16, /9 = 0 0 6 , analysis of the cell m e a n s s h o w e d this was due to great v a r l a b i h t y in the occipital r e s p o n s e T-tests p e r f o r m e d for b o t h the t e m p o r o p a r l e t a l a n d f r o n t a l responses Indicated t h a t there were no slgmflcant differences b e t w e e n amp h t u d e s at positrons 6 and 7 for e i t h e r of these sites, c o n g r u e n t w i t h the results from the o t h e ) s y n o n y m pair
19
ERP RESPONSE DECREMENT FRONTAL
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One stimulus pair in the lingmstlc class was composed of two words of different llngu]stic meanings but similar physical characteristics, being equated for size and brightness and sharing two of three letters (CUT/CUP) We predicted that early component responses to th~s pair would not exhibit response recovery because of the physical similarities, and that late c o m p o n e n t responses, especmlly from the temporopanetal site, would exhibit response recovery because of the semantic dlssimdarltles. For the early components, a significant effect of position appeared, F(3,21) = 5 28, p = 0.007, with both linear trends, F(1,7) = 8.06, p = 0.025, indicating that response recovery did not occur, and quadratic trends, F(1,7) = 8.75, p = 0 02, indicating that response recovery did occur Analysis of the cell means indicated that the quadratic trend was due to a large sensitized response at positron 6 (amphtude larger than that at poslhon 1) at the temporoparietal lead. The analysis of variance failed to show any slgmficant findings for the P3 component; however, a t-test showed, as predicted, a significant amplitude recovery, t(7) = 2 14, p < 0 05, at the temporoparletal lead. Therefore, results from this stimulus pair provide evidence for our lmtial hypothesis Table 1 shows the absolute amounts of amplitude change, m mlcrovolts, over positions 1 to 6 (amphtude at position 1 minus amphtude at posttmn 6) and over positions 6 to 7 (amphtude at pos]tlon 7 minus amplitude at position 6) at each electrode site for each stimulus pa]r. In general, the amplitude changes ranged from 1 to 6 mlcrovolts, indicating that the observed ERP changes were
based on substantial differences m amphtude across the stimulus positions.
Peak Latencws Although rather broad temporal windows were employed In determining peak components of the ERPs, both N~ P~ and P3 latencles fell within restricted portions of these windows Across stimulus pairs and electrode sites, the mean N, P2 latency was 206.1 msec, standard deviation = 29 3 msec, the mean P3 latency was 337 6 msec, standard devlatmn = 46 msec. Within stimulus pairs, there did not appear to be reliable differences between stimulus positions in latenc~es The standard error of the mean of the early and late latency averages across electrode sites, stimulus position and stimulus type was 8.2 msec for N~ P2 and 15 7 msec for P3. Thus, peak components appeared in restricted portions of the temporal windows and varied httle across condlhons
DISCUSSION Our results indicated that ERPs decrement in response to repeated stimulus presentations and recover to the introduction of a dlsslmtlar stimulus to varying degrees across electrode sites Moreover, early and late component response amphtudes did not always exhibit similar patterns of amplitude change; in fact, their differential sensitivity to st]mulus type was strikxng. Recent animal work [23,27] has similarly noted that amplitude decrements of separate
20
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FIG 4 Mean percentage amplitude changes over all st]mulus positions for three pairs of hnguIstlc stimuli. Response at posmon 1 has been set to 100%. Early (N~P~) and late (P3) component responses are presented separately. Each data point represents the mean amplitude over all subjects Electrode sites are F, left frontal T, left temporopanetal, and O, left occipital
e v o k e d p o t e n t i a l c o m p o n e n t s were i n d e p e n d e n t , c h a n g e s in l a t e r c o m p o n e n t s o f t e n o c c u r r i n g m the a b s e n c e o f syst e m a t i c c h a n g e s in earlier c o m p o n e n t s . Early c o m p o n e n t r e s p o n s e s to the hnguxstlc s t l m u h b e h a v e d in a m o r e u n i f o r m m a n n e r across e l e c t r o d e sites t h a n did t h e late c o m p o n e n t responses. O f the h n g u i s t l c pairs t h a t differed in p h y s i c a l c h a r a c t e r i s t i c s , all e x c e p t o n e pmr at one e l e c t r o d e l o c a t i o n ( L E A P / J U M P f r o m t h e f r o n t a l site) e v o k e d N~ P~ c o m p o n e n t s w h i c h e x h i b i t e d significant q u a d r a t i c t r e n d s over s t i m u l u s p o s i t i o n , 1.e., N, P~ d e c r e a s e d in r e s p o n s e t o t h e h a b i t u a t i o n s t i m u l u s b u t r e c o v e r e d in r e s p o n s e t o t h e g e n e r a l i z a t i o n stimulus. F o r the linguistic pair similar p h y s i c a l l y b u t dlssn-nilar s e m a n tically, a s l g m f l c a n t linear t r e n d over p o s i t i o n a p p e a r e d at t w o e l e c t r o d e sites T h e s e d a t a suggest t h a t N~ Pa was s e n s m v e to the sensory aspects of t h e stimuli T h e P3 c o m p o n e n t to linguistic s t i m u l i was sensitive to t h e s e m a n t i c c o n t e n t of the stimuli. Word pairs w i t h i d e n t i c a l
Note All amphtude measurements represent the mean change over all subjects N~P2 are early components, P3 are late ~omponents *Amphtude at position t minus amphtude at position 6 l.or negatwe values, amphtude at posmon 6 ]s larger than that at posmon l +Amphtude at posmon 7 minus amphtude at position 6 I.or negative values, amphtude at posmon 6 is larger than that at positron 7 or similar m e a n i n g s p r o d u c e d less r e s p o n s e r e c o v e r y ot t h e late c o m p o n e n t t h a n of t h e early c o m p o n e n t for t w o of the t h r e e s t i m u l u s pairs. This s e m a n t i c e f f e c t was p a r t i c u l a r l y n o t i c e a b l e in the t e m p o r o p a r i e t a l responses. T h e results for t h e linguistic pair w i t h dissimilar m e a n i n g s were n o t as clear-cut, h o w e v e r , t h e r e was some evidence t h a t the t e m p o r o p a n e t a l late c o m p o n e n t s were sensitive to the s e m a n t i c dissimilarity of these stimuli. Dissociation b e t w e e n the activity of early a n d late c o m p o n e n t s was also a p p a r e n t in the E R P s to t h e n o n linguistic s t l m u h . Early c o m p o n e n t responses generally d e c r e m e n t e d in r e s p o n s e to the h a b i t u a t i o n s t l m u h , m o s t c o n s i s t e n t l y at the occipital site. Occipital c o m p o n e n t s were quite sensitive to t h e sensory c h a r a c t e r i s t i c s of the stimuli, s h o w i n g r e s p o n s e r e c o v e r y to all g e n e r a h z a t : o n s t l m u h differing physically from the h a b i t u a h o n s t i m u h . F r o n t a l a n d t e m p o r o p a r i e t a l early c o m p o n e n t s were sun-
ERP R E S P O N S E D E C R E M E N T
21
darly sensltwe to all nonlinguishc pairs e x c e p t one. F o r the stimulus pair with no generalizahon sttmulus, a hxghly significant hnear effect of position appeared at all electrode s~tes. F o r b o t h the diffuse flashes of light and the simple geometric shapes, none of the P3 c o m p o n e n t s for any electrode site reflected rehable changes of stimulus t y p e or c o n t e n t . This was true even for the occipital late components On the other hand, slgmficant trends over s h m u l u s position did appear for the c o m p l e x nonlingulstlc stimuh. This result may reflect the c o m p l e x i t y rather than the nonhngulstlc nature of the stlmuh It must be n o t e d , however, that there were several nonsignificant trends ( 0 . 0 5 > p < 0 10) in the P3 c o m p o n e n t for b o t h stimulus position and electrode site With a larger sample size and m o r e stimulus presentations, several of these m a y b e c o m e significant F o r each stimulus pair, 5 F-tests were p e r f o r m e d on early and late c o m p o n e n t a m p h t u d e s , producing 90 total tests With such a large n u m b e r of tests, several comparisons might reach significance by chance. T w e n t y - o n e of our F-tests reached significance, including 12 at the 0.05 level, 7 at the 0.01 level and 2 at the 0.001 level. This n u m b e r is above chance e x p e c t a t i o n , and the significant results were in the predicted direction Our design i n c o r p o r a t e d predictable s h m u l u s changes, in that for each trial, subjects knew at what poslt~on the generalization stimulus would appear. It is possible that differential preparation or arousal affected the results, since after one sequence in a particular block, subjects would k n o w what the generalization stimulus was and could
prepare for it. F o r example, a recent study [28] showed that increased arousal, as indexed by a c o n t i n g e n t negative variation and an increased evoked potential, o c c u r r e d when relevant s t l m u h were m a d e predictable. On the o t h e r hand, we did find significant differences b e t w e e n responses at different scalp locations to the same stimulus pairs, which are n o t likely to be attributable to differences in arousal. The E R P changes to the bright/dim and d i m / b r i g h t flashes have relevance to accounts of intensity generallzatlon of habituation A c c o r d i n g to a dual-process theory of h a b i t u a t i o n [ 9 , 2 6 ] , a generahzation sttmulus of different intensity f r o m the h a b i t u a t i o n stimulus would produce different a m o u n t s of generalization depending on whether it was of higher or lower intensity than the h a b i t u a t i o n stimulus. The a m o u n t of generahzation was postulated to be a f u n c t i o n of the degree of overlap of excitation an the neural elements activated by the stimuh [ 2 4 ] . Therefore, increased intensity following h a b i t u a t i o n would yield a greater response because more elements would be activated; decreased intensity w o u l d yield either a small increase in response, no change, or a decrease, depending on specific e x p e r i m e n t a l parameters [ 2 6 ] . In the present study, early c o m p o n e n t s to the dim/bright flashes showed large amphrude increments to the bright flash at all electrode sites. Conversely, early c o m p o n e n t s to the bright/dim flashes recovered in amplitude to the dim flash only at the occipital p l a c e m e n t , showing little change at either frontal or t e m p o r o p a n e t a l placements These results support the dual-process theory, rather than theories predicting symmetrical changes in response to intensity differences [21]
REFERENCES 1. Butler, R.A. Effect of changes in stimulus frequency and intensity on habituation of the human vertex potential. J acoust. Soc. Am 4: 945-950, 1968. 2. Butler, R. A., M. Spreng and W. D. Keldel. Stimulus repetition rate factors which influence the auditory evoked potential. Psychophystology 5: 665-672, 1969. 3. CaUaway, E., III. Habituation of averaged evoked potentials in man. In Habituatton, Vol II, Physiologwal Substrates, edited by H V. S Peeke and M J Herz. New York: Academic Press, 1973, pp. 153-174. 4. Davis, H., T. Mast, N Yoshle and S. Zerhn. The slow response of the human cortex to auditory stlmuh: Recovery process. Electroenceph chn Neurophyszol 21: 105-113, 1966. 5 Dlmond, S. J and J . G Beaumont (Eds.). Hemtsphere Functzon m the Human Brain New York. Halsted Press, 1974. 6. Dixon, W.J Btomedwal Computer Programs. Berkeley' University of California Press, 1975 7. Fruhstorfer, H Habituation and dlshabituatlon of the human vertex response. Electroenceph chn Neurophystol 30: 306-312, 1971. 8 Fruhstorfer, H , P. Soven and T. Jarvflehto Short-term habituation of the auditory evoked response m man. Electroenceph chn Neurophystol 28: 153-161, 1970 9. Groves, P.M. and R . F . Thompson. Habituation" A dual process theory Psychol. Rev. 77: 419-450, 1970. 10. Jasper, H.H. The ten-twenty electrode system of the raternational federation. Electroenceph clin. Neurophyslol 10: 371-375, 1958. 11 Johnston, V S and G.L. Chesny Electrophysiological correlates of meaning. Science 186: 944-946, 1974. 12 Maclean, V., A. Ohman and M. Lader Effects of attention, activation and stimulus regularity on short-term habituation of the averaged evoked potential. Blol Psychol. 3: 57-69, 1975.
13 14. 15.
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21 22.
Morrell, L. K. and J. G. Salamy Hemispheric asymmetry of electrocortical responses to speech stlmuh. Scwnce 174: 164-166, 1971. Ohman, A. and M. Lader. Selective attention and "habituation" of the auditory averaged evoked response m humans. Physiol. Behav 8: 79-85, 1972. Ohman, A., V. Maclean and M. Lader. Concomitant short-term changes in the auditory evoked response, the EEG, and reaction-time performance m relation to the temporal parameters of stimulation. Scand J Psychol 16: 177-183, 1975. Peeke, H V. S. and M J. Herz. Habttuation, Vol. 1, Behavioral Studies, Vol. II, Physiologwal Substrates. New York' Academic Press, 1973. Regan, D Evoked Potenttals m Psychology, Sensory Phystology and Chnical Medwme. London: Chapman and Hall, 1972 Rltter, W, H. G. Vaughan, Jr. and L. D. Costa Orienting and habituation to auditory stimuli: A study of short term changes m average evoked responses. Electroenceph chn. Neurophysiol. 25: 550-556, 1968. Rltter, W. and H. G. Vaughan, Jr Averaged evoked responses m vigilance and discrimination" A reassessment Sctence 164: 326-328, 1969 Schandry, R , N. Blrbaumer and W Lutzenberger. Analys~s of habituation of the components of the auditory evoked potential to stlmuh of different intensities. Psychophysiology 14: 105-106, 1977 Sokolov, Y. N. Perceptton and the Conditioned Reflex New York MacMdlan, 1963. Sutton, S The specification of psychological variables m an average evoked potential experiment In Average Evoked Potentials Methods, Results and Evaluations, edited by E Donchm and D B Llndsley Washington, D C NASA, 1969, pp 237-298.
22
23.
24
25
26
M t ~ ; F I _ A , T[-'~ I F R
Teyler, T J , R A Roemer and R t T h o m p s o n Habituation o f the pyramidal response in unanesthetJzed cat Phv~tol Behav 8 : 2 0 1 205, 1972 T h o m p s o n , R F The neural basis of s n m u l u s generahzatlon In Stimulus generahzanon, edited by D I Mostotsky Stanford. Stanford University Press, 1965, pp 154 178. T h o m p s o n , R I and W A Spencer. Habituation. A model p h e n o m e n o n for the study of neuronal substrates ot behavior Psychol. Rev 7 3 : 1 6 43, 1966 T h o m p s o n , R. F , P M. Groves, T J. Teyler and R A Roemer A dual-process theory o f h a b l t u a n o n Theory and behavmr In, Habttuatton. Vol I, Behavioral Studies, edited by H V S Peeke and M J Herz New York Academmc Pre~s, 1973, pp 239--271
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28
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Westenberg. 1 S , (; Patge, B Golub ,rod N \1 \~.cmi~cr~: Fvoked potential decremenls m aud~tor~, ~.(~e\ I l h ~ r ¢ l e rlal and ~ ontlnual ~tlmulatlon IL'[(~l'~¢t()('t?( t [711 , [l~ Neuroph_rstol 4 0 : 3 3 7 355, 1976 Wdkmson, R F and S M Ashby Selectl~c ~ttlellll,,n, Lontlngent negdlwe variation and the ew~ked potential t:]l~p[ Psrchol 1 : 1 6 7 179, 1974 Wmer, B J Stattstwal Prtnclples In Expertmental D¢'~tcp~. second edlnon New "~ork McGra~-Hill, 1971
ERP Response Decrement and Recovery as a Function of Stimulus Type and Scalp Locatioff A N D R E A L. M E G E L A 2, T I M O T H Y J. T E Y L E R 3 A N D G A R Y W. H E S S E
Department o f Psychology and Social Relations, Harvard University, Cambridge, MA 02138 (Received 10 D e c e m b e r 1976) MEGELA, A. L., T. J. TEYLER AND G. W. HESSE. ERP response decrement and recovery as a functlon of sttmulus type and scalp location PHYSIOL. BEHAV. 19(1) 15-22, 1977. - - Response decrement and recovery of visual event-related potentials (ERPs) at different electrode sites to different types of repetitive stimuli were studied. Nine blocks of stimuli were presented in the form AAAAAABB. Stimuli were of four types: diffuse flashes of light, geometric shapes, words of similar meanings, and words of dissimilar meanings. The relative amounts of ERP response decrement and recovery differed as a function of ERP response components measured (early vs. late), electrode site (left frontal, left temporoparietal, and left occipital), and stimulus type. Early components were sensitive to sensory characteristics of the stimuli. Late components from the left temporoparletal site were sensitive to the meanings of the linguistic stimuh. The research suggests a useful paradigm for the study of habituation-like responses and of cerebral specificity in an intact normal population. Event-related potentials Intensity generalization
Visual evoked potentials Habituation
Response decrement
WE H A V E e m p l o y e d a h a b i t u a t l o n / g e n e r a h z a t i o n paradigm in an a t t e m p t to examine differences in l n t r a h e m l s p h e n c event-related potentials (ERPs) to several classes of hngulstlc and n o n h n g m s t l c stimuli. R e c e n t l y , it has been d e m o n s t r a t e d that ERPs recorded from the h u m a n scalp exhibit several of the parametric features of h a b i t u a t i o n as defined by T h o m p s o n and Spencer [ 2 5 ] . These include a m p h t u d e d e c r e m e n t s following a negative e x p o n e n t i a l f u n c t i o n ; s p o n t a n e o u s recovery, the direct relation b e t w e e n stimulus f r e q u e n c y and degree o f h a b i t u a t i o n , the inverse relation b e t w e e n stimulus intensity and degree of habituation, and stimulus generahzatlon [1, 2, 3, 4, 7, 8, 12, 14, 15, 16, 18, 2 0 ] . All of the parametric features of h a b i t u a t i o n have not, however, been observed m the ERP, suggesting caution m interpreting these results as an instance of habituation. Since the ERPs in the present study are n o t e x a m i n e d for all of the parametric features of habituation, we shall e m p l o y the m o r e conservatwe term response d e c r e m e n t The d e m o n s t r a t i o n that ERPs exhibit response dec r e m e n t and recovery m a h a b i t u a t i o n / g e n e r a l i z a t i o n paradigm is of interest for several reasons. First of all, differing theoretical predictions concerning the nature of h a b i t u a t i o n [9, 21, 25] could be tested with this paradigm. F u r t h e r m o r e , by recording ERPs from several different scalp locations, cerebral locahzat~on and f u n c t i o n in an
Cerebral specificity
intact normal population could be investigated, with a m e t h o d wh,ch c o m p l e m e n t s and extends previous research based on behavioral measures (e g., [ 5 ] ). The procedure used m this study revolved the rapid presentatxon of a series of identical stxmuh followed by a test stimulus differing on one or m o r e dimensions. The ERP response to the repeated identical stimuli (the h a b i t u a t i o n stimuh) was e x p e c t e d to decrement. The degree to which ERPs to the h a b i t u a t i o n and test (generahzatlon) stlmuh were related reflected the underlying cerebral processing of the two stimulus types If the a m p h t u d e of the ERP to the generahzatlon stimulus was equal to or smaller than the amplitude of the ERP to the last habltuat~on stimulus of the series (e.g., the response remained d e c r e m e n t e d ) , we assumed that the two stlmuh were being processed similarly. Conversely, xf the response to the generahzatlon stimulus was larger than that to the last habituataon stimulus of the series (e g., the response recovered), we assumed that the two stimuli were being processed differently. The relative a m o u n t s of response change represent an index of the degree to which a specific cortical site is processing the difference b e t w e e n the stlmuh. F o r example, a similar response to two different stlmuh indicates that the dimension across which the stimuli differ is n o t being processed at that s~te. We hypothesized that the relative a m o u n t s of ERP
1Supported by an N.I.M.H predoctoral fellowship and a grant from the Department of Psychology and Social Relations, Harvard University, to the first author, and a grant from the Milton Fund of Harvard Umversity to the second author. We thank P Clark, R. H. Dworkln, R, Hastie and L. Teyler for their valuable assistance. 2Now at the Section of Neurobiology and Behavior, Largmutr Laboratory, Comell University, Ithaca, New York 14853 Send reprint requests to this address. 3 Now at the Neurobtology Program, Northeastern Ohio Universities College of Medicine, Rootstown, Ohio 44272. 15
16
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r e s p o n s e d e c r e m e n t and r e c o v e r y would differ as a t u n c t l o n of e l e c t r o d e scalp l o c a t i o n (left f r o n t a l , left telnporoparaetal or left occipital), s t i m u l u s t y p e (linguistic or n o n h n g u l s t l c ) , a n d the specific E R P c o m p o n e n t m e a s u r e d {early or l a t e ) We p r e d i c t e d t h a t early c o m p o n e n t s , o c c u r r i n g b e t w e e n 50 a n d 250 msec p o s t s t i m u l u s o n s e t , w o u l d process the sensory aspects o f b o t h linguistic and n o n h n g u i s t l c s t i m u h , especially at the o c c i p i t a l l o c a t i o n , in a c c o r d w i t h p r e v i o u s w o r k o n visual e v o k e d p o t e n t i a l s [ 1 7 ] . Late c o m p o n e n t s , o c c u r r i n g b e t w e e n 2 5 0 a n d 4 0 0 msec p o s t s t l m u l u s o n s e t , were e x p e c t e d to be less sensitive to the sensory aspects and m o r e sensitive to the s e m a n t i c aspects of t h e h n g u l s t l c stimuli, since these c o m p o n e n t s are b e i n g r e c o r d e d f r o m t h e left h e m i s p h e r e and have b e e n s h o w n to be sensitive to cognitive and h n g u l s t l c variables [ 11, 19, 221 F o r e x a m p l e , w i t h a pair of linguistic stimuli of Identical m e a n i n g s b u t d i f f e r e n t physical characteristics, t h e occipital early c o m p o n e n t s w o u l d be e x p e c t e d to show r e s p o n s e r e c o v e r y because o f the physical d i f f e r e n c e s b e t w e e n the stimuli The t e m p o r o p a r a e t a l late c o m p o n e n t responses, p r e s u m a b l y reflecting activity f r o m areas of the left h e m i s p h e r e i m p o r t a n t for language r e c e p t i o n [ 1 3 ] , would r e m a i n d e c r e m e n t e d to these t w o s t i m u h o f i d e n t i c a l m e a n i n g . On t h e o t h e r h a n d , for n o n h n g u l s t l c stimuli of d i f f e r e n t physical characteristics, occipital, t e m p o r o p a r l e t a l a n d f r o n t a l early c o m p o n e n t s w o u l d all be e x p e c t e d to show r e c o v e r y of r e s p o n s e to the g e n e r a h z a t l o n s t i m u l u s if early c o m p o n e n t left h e m i s p h e r e ERPs e n c o d e o n l y physical aspects of nonlanguastlc stlmUh Late c o m p o n e n t E R P r e s p o n s e s w o u l d n o t be e x p e c t e d to show recovery to nonhnguastac g e n e r a h z a t I o n stimuli if these r e s p o n s e s are n o t sensitive to n o n h n g u l s t l c stimuli METHOD
T h r e e m a l e s a n d seven females, aged 19 33 years, p a r t i c i p a t e d in t h e e x p e r i m e n t All were r i g h t - h a n d e d , w i t h n o f a m i l y h i s t o r y of l e f t - h a n d e d n e s s . E a c h subject part l c i p a t e d in a single e x p e r i m e n t a l sessmn lasting a p p r o x i m a t e l y t w o hr. E E G was r e c o r d e d f r o m t h r e e scalp l o c a t i o n s F3, 01, and a t e m p o r o p a r i e t a l p l a c e m e n t equid i s t a n t b e t w e e n C3, T3 a n d P3 ( I n t e r n a t i o n a l 1 0 - 2 0 system, [ 1 0 1 ) E l e c t r o d e s were m i n i a t u r e B e c k m a n silversilver c h l o r i d e , held in place b y a s t r e t c h a b l e lycra cap w o r n b y the subjects. L i n k e d ears served as r e f e r e n c e , a n d a f o r e a r m e l e c t r o d e served as g r o u n d Eye m o v e m e n t s were r e c o r d e d f r o m e l e c t r o d e s p l a c e d lateral to and u n d e r n e a t h the right eye. All e l e c t r o d e resistances were k e p t b e l o w 10 k a E E G a n d E O G activity were a m p l i f i e d t h r o u g h a Grass M o d e l 7 p o l y g r a p h ( b a n d p a s s 1 - 3 5 c/sec) and r e c o r d e d o n FM tape for off-line analysis by a PDP-9 c o m p u t e r . E E G was averaged at a s a m p l i n g rate o f 512 c/sec for 5 0 0 msec e p o c h s b e g i n n i n g w i t h s t i m u l u s onset. Stimuli were p r e s e n t e d b y t w o slide p r o j e c t o r s e q u i p p e d w i t h G e r b r a n d s t a c h l s t o s c o p l c s h u t t e r s activated b y Massey-Dickinson programming equipment To avoid a u d i t o r y c o n t a m i n a t i o n o f the visual ERPs, the noise o f the s h u t t e r s was m a s k e d b y b a c k g r o u n d w h i t e noise Simu l t a n e o u s w i t h s h u t t e r o p e n i n g , a 2 V, 5 0 0 msec pulse also a c t i v a t e d by the p r o g r a m m i n g e q u i p m e n t was placed o n tape a n d s u b s e q u e n t l y used to trigger t h e c o m p u t e r for E R P averaging. S t l m u h were b a c k - p r o j e c t e d o n t o a screen in a s o u n d - d e a d e n i n g r e c o r d i n g c h a m b e r in w h i c h s u b j e c t s were seated
The e x p e r i m e n t a l s e s s I o n consisted t~l t l l r l t ~ S C p d [ a { ~ b l o c k s of s t l m u h Each b l o c k was c o m p o s e d of t w o s t m l u : J , A and B, p r e s e n t e d in the s e q u e n c e A A A A & a , BB S1Hnulu~ A was the h a b i t u a t i o n stimulus, s t i m u l u s B was ~tle g e n e r a l i z a t i o n s t i m u l u s Within each block, average~ ~ e r c m a d e t r o m the h r s t 10 artifact-free stmmlu~ wquetices, w i t h a m a x i m u m of 15 s e q u e n c e s being p r e s e n t e d pel b l o c k This relatively small n u m b e r of s t i m u l u s r e p e t i t i o n s was c h o s e n to lessen the total time ol the e x p e N m e n t a t session m o r d e r to avoid subject fatigue and any pOsblble s t i m u l u s satiat~on effects W~thln each s t u n u l u s s e q u e m e , the l n t e r s t i m u l u s lnterx.al was 1600 msec t'ach 800 nlsec d u r a t m n s t i m u l u s being p r e c e d e d by an 800 msec i i x a t l o n p o i n t T h e interval b e t w e e n s t i m u l u s s e q u e n c e s w i t h i n a b l o c k varied b e t w e e n 10 and 12 sec, while the lntelval b e t w e e n b l o c k s was a p p r o x i m a t e l y 5 m m Fhe order ol s t i m u l u s blocks was r a n d o m l z e d for each sublect S u b j e c t s were n o t r e q u i r e d to r e s p o n d to the s t l m u h T h e y were i n s t r u c t e d , h o w e v e r , to avoid gross bodily m o v e l n e n t s and e y e b h n k s a n d to m a i n t a i n tLxation during p r e s e n t a t i o n ol stimuli P o l y g r a p h records weie e x a m i n e d lor these sources of c o n t a m i n a t i o n and the trials e h m i n a l e d from the average The relatively sho~t time span ot each stimulus b l o c k h e l p e d to ensure t h a t subjects r e m a i n e d a(tenll~e d u r i n g each b l o c k The nine d i f f e r e n t s t i m u l u s pairs r e p r e s e n t e d three classes n o n h n g u l s t l c s t l m u h (5 pair), linguistic stimuli of similar or identical m e a n i n g s (3 pair), and hngulstlc s t m l u h of d i f f e r e n t m e a n i n g s b u t slinllar physical c h a r a c t e r i s t i c s l 1 pair) The n o n h n g u l s t l C stimuli were h n e drawlng~ ot varying c o m p l e x l t } t h a t were n o t easily e n c o d e d verbally and diffuse flashes of light Linguistic stltnuh ot smlflar m e a n i n g s were s y n o n y m s , linguistic s t i m u h oI identical m e a n i n g s consisted ol the same word p r e s e n t e d in d i f f e r e n t t y p e f o n t s Linguistic s t l m u h of d i f f e r e n t m e a n i n g s were c h o s e n to be very sm~ilar along every d i m e n s i o n e x c e p t s e m a n t i c E x c e p t for the diffuse flashes ot light, l u m i n a n c e level was e q u a t e d w i t h i n each pair of SlllnUll The nine d i f f e r e n t s t i m u l u s pairs are s h o w n in Table 1 4 s ~an be seen from this table, in one s t i m u l u s block ( n o n l l n g u l s t l c geometrlc}, no generalization stimulus appeared In a d d i t i o n , t w o n o n h n g u l s t l c blocks were c o m p o s e d o1 the same pmr of stimuli b u t p r e s e n t e d in d i f f e r e n t positions, 1.e, A A A A A A B B and B B B B B B A A f o r m e d the two diff e r e n t blocks This was also true of t w o llngmstlc b l o c k s Within each s t i m u l u s block, average 1~RPs were c o m p u t e d across s t n n u l u s s e q u e n c e s for stimuli nl p o s i t i o n n u m b e r s 1, 4, 6, and 7 t t h e first g e n e r a l t z a t m n .~tmmlus} This p r o d u c e d a s t i m u l u s - b y - s t i m u l u s average consisting of all initial stamuh w i t h i n a p a r t i c u l a r block, all f o u r t h stimuli, etc, (see [ 1 8 ] ) After averaging, the ERPs were p h o t o g r a p h e d f r o m a c o m p u t e r slave screen These p h o t o graphs were enlarged and m e a s u r e d to o b t a i n c o m p o n e n t a m p l i t u d e s All a m p l i t u d e m e a s u r e m e n t s were m a d e in a b l i n d m a n n e r , the scorer b e i n g u n a w a r e uf s t i m u l u s type, e l e c t r o d e l o c a t i o n or s t i m u l u s p o s i t i o n for any ot the ERPs F o r each ERP, two c o m p o n e n t s were m e a s u r e d peakt o - p e a k a m p l i t u d e s of N, P~, defined as the largest negative-positive d e f l e c t m n in the latency ~ange 5 0 - 2 5 0 msec, a n d b a s e h n e - t o - p e a k a m p l i t u d e of P3, defined as the largest positive d e f l e c t i o n relative to baseline in the latency range 250 4 0 0 msec These relatively b r o a d l a t e n c y ranges were c h o s e n because of the great i n t e r and lntraindavidual variability e x p e c t e d in the ERPs across t h e d i f f e r e n t s t l m u h used A c t u a l r e s p o n s e latencies of c o m p o n e n t peaks within
ERP RESPONSE DECREMENT
17
each temporal window were substantially less broad; the values are reported below. For each stimulus pair, early and late c o m p o n e n t amplitudes were separately analyzed by a two-way repeated measures analysis of variance (ANOVA) [6,29] with electrode sites and stimulus position as the repeated measures. Eighteen separate ANOVAs were computed. For each ANOVA, five F-tests were computed - main effects for site and for position, hnear and quadratic trends for position, and the site by position interaction. Linear and quadratic trend analyses were performed in order to assess the profile of amplitude change across stimulus position. In this design, a linear trend implies a consistent decrease in amplitude across stimulus position, while a quadratic trend implies a decrease followed by recovery [29]. Although all nine stimulus blocks were presented to each subject, eyebhnks, eye movement, or muscle artifacts forced ehm1nation of at least one block for 8 of the 10 subjects The different number of subjects for each ANOVA and the analyses for trend components are reflected in the different degrees of freedom for the F-ratios (degrees of freedom are reported along with F values) RESULTS
Nonhngutstlc Sttmu h Sample ERP waveforms superimposed~ for all subjects from one pair of nonhnguistlc stimuli are presented m Fig 1 Mean percentage changes in amplitude of early and
FRONTAL
late components for three pairs of nonlinguistlc stimuli are shown in Fig. 2 Two flashes of different brJghtnesses, counterbalanced for direction of brightness change, served as stimuli. For the dim/bright pair, the N 1 P2 components showed response decrement to the dim flash and response recovery to the bright flash as shown by a mare effect for position, F(3,27) = 5.01, p = 0.007, with a significant quadratic trend, F(1,9) = 2 1 . 3 2 ; p = 0.001 For the bright/dim flashes, the occipital responses recovered in response to the dim flash while the temporoparletal and frontal leads showed no significant response recovery, F(6,42) = 2 32; p = 0.05 Thus, when the generalization stimulus was brighter or dimmer than the habituation stimulus, occipital early components processed this difference, whale frontal and temporoparietal early components did so only In the case of the brighter generalization flash Late components for both pairs of flashes evidenced nonsignificant quadratic trends for position This suggests that P3 components from both anterior and posterior left hemisphere sites may not reliably process brightness differences between these nonllngulstlc stlmuh Early component ERPs at all sites to the simple line drawings decremented over stimulus positions 1 to 6, F(3,24) = 3.84; p = 0.02, and recovered in response to the generalization stimulus (quadratic trend, F ( 1 , 8 ) = 5.49, p < 0 05). A main effect for site, F(2,16) = 6 . 6 4 ; p = 0 008, indicated that a relatively greater amount of response decrement and more recovery occurred at the temporo-
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FIG 2. Mean percentage amplitude changes over all stimulus positions for three pairs of nonllngmstlc stimuli. Response at position l has been set to 100% Early (NIP~) and late (P3) component responses are presented separately Each data point represents the mean amplitude over all subjects Electrode sites are F, left frontal; T, left temporoparIetal, and O, left occipital
parietal lead P a t t e r n s of a m p h t u d e change for the P3 c o m p o n e n t were n o t s~gmflcant Early c o m p o n e n t r e s p o n s e s to t h e c o m p l e x g e o m e t r i c shapes s h o w e d a significant q u a d r a t i c t r e n d over s t i m u l u s p o s i t r o n , F ( 1 , 8 ) = 10.36, p = 0 01, and a m a r e effect for s~te, F ( 2 , 1 6 ) = 7 . 2 9 ; p = 0 006, w i t h little a m p h t u d e c h a n g e o c c u r r i n g at the t e m p o r o p a r l e t a l lead Late c o m p o n e n t r e s p o n s e s to this s h m u l u s pair, u n l i k e t h o s e to t h e o t h e r n o n h n g m s t l c pmrs, also e x h i b i t e d a s l g m f l c a n t m a r e e f f e c t for p o s i t r o n , F ( 3 , 2 4 ) = 3 16, p = 0 04, w i t h a s~gnlflcant quadratic trend, F(1,8)= 5 75, p = 0 0 4 , the f r o n t a l r e s p o n s e r e c o v e r i n g m o r e t h a n the o t h e r responses. Th~s suggests t h a t t h e f r o n t a l E R P s m a y have b e e n processing c o m p l e x i t y or n o v e l t y of the s h m u h , r a t h e r t h a n t h e i r n o n h n g u l s t l c n a t u r e per se Finally, a n o - c h a n g e c o n d i t i o n , in w h i c h the same simple h n e d r a w i n g a p p e a r e d m all m g h t s t i m u l u s p o s i t i o n s per s e q u e n c e , was i n c o r p o r a t e d in the design As p r e d i c t e d , a r o b u s t l i n e a r e f f e c t for positron, md~catlng c o n t i n u e d d e c r e m e n t o f r e s p o n s e for all 8 s t i m u l u s p o s m o n s , o c c u r r e d for early c o m p o n e n t s , F ( 1 , 6 ) = 4 0 6 6 , p = 0 001 A m a i n e f f e c t of s~te, F ( 2 , 1 2 ) = 7 3 9 , p = 0 0 0 8 , suggested t h a t the
S a m p l e ERP w a v e f o r m s l r o m all subjects for one pair ol linguistic s t l m u h are p r e s e n t e d in Fig 3 Mean p e r c e n t a g e changes m a m p l i t u d e of early and late c o m p o n e n t s toJ t h r e e pairs ot linguistic s t l m u h are p r e s e n t e d in F~g 4 Early a n d late c o m p o n e n t ~ e x h i b i t e d d i f f e r e n t p a t t e r n s of a m p l i t u d e change in response to the hnguistlc stamuh N 1 P: a m p l i t u d e s to the s h m u l u s pmr identical m m e a n i n g b u t differing in physical c h a r a c t e n s h c s ( d o g / D O G ) s h o w e d a s]gnlflcant mare effect ol pos]tion, F ( 3 , 2 4 ) = 3 3 8 , p = 0 0 3 , with a q u a d r a t i c t r e n d , F ( 1 , 8 ) = 5 5b, p < 0 0 5 . m d l c a t l n g r e s p o n s e d e c r e m e n t over p o s i U o n s 1 to 0, wiltl recovery o c c u r r i n g to the g e n e r a h z a t i o n s t i m u l u s Thus, all e l e c t r o d e sites were r e s p o n s w e to the ph~cslcal dJlferenee~ b e t w e e n these t w o s h m u h A o n e - t a f l e d t - t e s t t o r c o r r e l a t e d m e a n s [29] i n d i c a t e d t h a t significantly greater recover3 ol r e s p o n s e o c c u r r e d at occipital t h a n at frontal or t e m p o r o parietal sites, t ( 8 ) = 3 08. p . 0 0 1 P3 a m p h t u d e s from t e m p o r o p a r i e t a l and f r o n t a l sites to this s t i m u l u s pair. w h d e again d e c r e m e n t i n g over p o s i t i o n s 1 to 6, did n o t ~ignfflcantly recover In response to the g e n e r a l i z a t i o n q~rnulus The m a i n e t l e c t f o r p o s m o n , F ( 3 , 2 4 ) = 3 8 7 , / 9 = 0 0 2 , a p p e a r e d with only a marginally significant linear t r e n d , F(1,8) = 464, p = 00b T-tests s h o w e d a s l g m h c a n t increase in r e s p o n s e to the g e n e r a l i z a t i o n ~txmulus at the occipital lead, t ( 8 ) = 1 95, p 0 0 5 , w i t h t e m p o r o p a n c l a I and f r o n t a l leads e x h i b i t i n g httle r e c o v e r y to that stlmulu.~ This suggests t h a t , as with several of the n o n l l n g m s t l e s t l m u h , P3 c o m p o n e n t s did n o t reliably process physical differences, h o w e v e r , as p r e d i c t e d , P3 c o m p o n e n t s lronl ~rontal a n d t e m p o r o p a r l e t a l sites were ~cns~t~ve to the s e m a n h c f e a t u r e s ol these ~timuh S e m a n t i c elfe~ts were l u r t h e r investigated w~th the s y n o n y m pairs ol Stllnuh l n t e r p r e t a t m n of these Jesuits, h o w e v e r , m u s t be viewed with c a u t i o n , as the t r e n d s o b s e r v e d were n o t s y m m e t r i c a l b e t w e e n the two pmrs F o r one pair ( J U M P / L E A P ) , early c o m p o n e n t s significantly c h a n g e d over s h m u l u s posit]on, F ( 3 , 2 1 ) = 3 0 7 , / 9 = 0 05 with a q u a d r a t i c t r e n d a c c o u n t i n g for the effect at all e l e c t r o d e sites F o r the reverse pair (LEAP~JUMP), this result held true for the occipital and t e m p o r o p a r i e t a l s~tes only, as s h o w n by a m a i n effect for site, F ( 2 , 1 6 ) = 4 4 2 , p = 0 03 T h u s , m general, early c o m p o n e n t s were n o t ~cns]tlve to the s e m a n t i c similarity b e t w e e n these s t l m u h As p r e d i c t e d , P3 c o m p o n e n t s to one s y n o n y m pair ( J U M P / L E A P ) e v i d e n c e d a r o b u s t h n e a r effect over stimulus p o s i t i o n , F ( I , 7 ) = 10.76, p = 0.01, all ot the lead~ s h o w i n g h t t l e r e s p o n s e recovery to s h m u l u s 7 F o r the reverse s y n o n y m pair, a marginally slgmflcant site by p o s i t r o n i n t e r a c t i o n a p p e a r e d , F ( 6 , 4 8 ) = 2 16, /9 = 0 0 6 , analysis of the cell m e a n s s h o w e d this was due to great v a r l a b i h t y in the occipital r e s p o n s e T-tests p e r f o r m e d for b o t h the t e m p o r o p a r l e t a l a n d f r o n t a l responses Indicated t h a t there were no slgmflcant differences b e t w e e n amp h t u d e s at positrons 6 and 7 for e i t h e r of these sites, c o n g r u e n t w i t h the results from the o t h e ) s y n o n y m pair
19
ERP RESPONSE DECREMENT FRONTAL
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One stimulus pair in the lingmstlc class was composed of two words of different llngu]stic meanings but similar physical characteristics, being equated for size and brightness and sharing two of three letters (CUT/CUP) We predicted that early component responses to th~s pair would not exhibit response recovery because of the physical similarities, and that late c o m p o n e n t responses, especmlly from the temporopanetal site, would exhibit response recovery because of the semantic dlssimdarltles. For the early components, a significant effect of position appeared, F(3,21) = 5 28, p = 0.007, with both linear trends, F(1,7) = 8.06, p = 0.025, indicating that response recovery did not occur, and quadratic trends, F(1,7) = 8.75, p = 0 02, indicating that response recovery did occur Analysis of the cell means indicated that the quadratic trend was due to a large sensitized response at positron 6 (amphtude larger than that at poslhon 1) at the temporoparietal lead. The analysis of variance failed to show any slgmficant findings for the P3 component; however, a t-test showed, as predicted, a significant amplitude recovery, t(7) = 2 14, p < 0 05, at the temporoparletal lead. Therefore, results from this stimulus pair provide evidence for our lmtial hypothesis Table 1 shows the absolute amounts of amplitude change, m mlcrovolts, over positions 1 to 6 (amphtude at position 1 minus amphtude at posttmn 6) and over positions 6 to 7 (amphtude at pos]tlon 7 minus amplitude at position 6) at each electrode site for each stimulus pa]r. In general, the amplitude changes ranged from 1 to 6 mlcrovolts, indicating that the observed ERP changes were
based on substantial differences m amphtude across the stimulus positions.
Peak Latencws Although rather broad temporal windows were employed In determining peak components of the ERPs, both N~ P~ and P3 latencles fell within restricted portions of these windows Across stimulus pairs and electrode sites, the mean N, P2 latency was 206.1 msec, standard deviation = 29 3 msec, the mean P3 latency was 337 6 msec, standard devlatmn = 46 msec. Within stimulus pairs, there did not appear to be reliable differences between stimulus positions in latenc~es The standard error of the mean of the early and late latency averages across electrode sites, stimulus position and stimulus type was 8.2 msec for N~ P2 and 15 7 msec for P3. Thus, peak components appeared in restricted portions of the temporal windows and varied httle across condlhons
DISCUSSION Our results indicated that ERPs decrement in response to repeated stimulus presentations and recover to the introduction of a dlsslmtlar stimulus to varying degrees across electrode sites Moreover, early and late component response amphtudes did not always exhibit similar patterns of amplitude change; in fact, their differential sensitivity to st]mulus type was strikxng. Recent animal work [23,27] has similarly noted that amplitude decrements of separate
20
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FIG 4 Mean percentage amplitude changes over all st]mulus positions for three pairs of hnguIstlc stimuli. Response at posmon 1 has been set to 100%. Early (N~P~) and late (P3) component responses are presented separately. Each data point represents the mean amplitude over all subjects Electrode sites are F, left frontal T, left temporopanetal, and O, left occipital
e v o k e d p o t e n t i a l c o m p o n e n t s were i n d e p e n d e n t , c h a n g e s in l a t e r c o m p o n e n t s o f t e n o c c u r r i n g m the a b s e n c e o f syst e m a t i c c h a n g e s in earlier c o m p o n e n t s . Early c o m p o n e n t r e s p o n s e s to the hnguxstlc s t l m u h b e h a v e d in a m o r e u n i f o r m m a n n e r across e l e c t r o d e sites t h a n did t h e late c o m p o n e n t responses. O f the h n g u i s t l c pairs t h a t differed in p h y s i c a l c h a r a c t e r i s t i c s , all e x c e p t o n e pmr at one e l e c t r o d e l o c a t i o n ( L E A P / J U M P f r o m t h e f r o n t a l site) e v o k e d N~ P~ c o m p o n e n t s w h i c h e x h i b i t e d significant q u a d r a t i c t r e n d s over s t i m u l u s p o s i t i o n , 1.e., N, P~ d e c r e a s e d in r e s p o n s e t o t h e h a b i t u a t i o n s t i m u l u s b u t r e c o v e r e d in r e s p o n s e t o t h e g e n e r a l i z a t i o n stimulus. F o r the linguistic pair similar p h y s i c a l l y b u t dlssn-nilar s e m a n tically, a s l g m f l c a n t linear t r e n d over p o s i t i o n a p p e a r e d at t w o e l e c t r o d e sites T h e s e d a t a suggest t h a t N~ Pa was s e n s m v e to the sensory aspects of t h e stimuli T h e P3 c o m p o n e n t to linguistic s t i m u l i was sensitive to t h e s e m a n t i c c o n t e n t of the stimuli. Word pairs w i t h i d e n t i c a l
Note All amphtude measurements represent the mean change over all subjects N~P2 are early components, P3 are late ~omponents *Amphtude at position t minus amphtude at position 6 l.or negatwe values, amphtude at posmon 6 ]s larger than that at posmon l +Amphtude at posmon 7 minus amphtude at position 6 I.or negative values, amphtude at posmon 6 is larger than that at positron 7 or similar m e a n i n g s p r o d u c e d less r e s p o n s e r e c o v e r y ot t h e late c o m p o n e n t t h a n of t h e early c o m p o n e n t for t w o of the t h r e e s t i m u l u s pairs. This s e m a n t i c e f f e c t was p a r t i c u l a r l y n o t i c e a b l e in the t e m p o r o p a r i e t a l responses. T h e results for t h e linguistic pair w i t h dissimilar m e a n i n g s were n o t as clear-cut, h o w e v e r , t h e r e was some evidence t h a t the t e m p o r o p a n e t a l late c o m p o n e n t s were sensitive to the s e m a n t i c dissimilarity of these stimuli. Dissociation b e t w e e n the activity of early a n d late c o m p o n e n t s was also a p p a r e n t in the E R P s to t h e n o n linguistic s t l m u h . Early c o m p o n e n t responses generally d e c r e m e n t e d in r e s p o n s e to the h a b i t u a t i o n s t l m u h , m o s t c o n s i s t e n t l y at the occipital site. Occipital c o m p o n e n t s were quite sensitive to t h e sensory c h a r a c t e r i s t i c s of the stimuli, s h o w i n g r e s p o n s e r e c o v e r y to all g e n e r a h z a t : o n s t l m u h differing physically from the h a b i t u a h o n s t i m u h . F r o n t a l a n d t e m p o r o p a r i e t a l early c o m p o n e n t s were sun-
ERP R E S P O N S E D E C R E M E N T
21
darly sensltwe to all nonlinguishc pairs e x c e p t one. F o r the stimulus pair with no generalizahon sttmulus, a hxghly significant hnear effect of position appeared at all electrode s~tes. F o r b o t h the diffuse flashes of light and the simple geometric shapes, none of the P3 c o m p o n e n t s for any electrode site reflected rehable changes of stimulus t y p e or c o n t e n t . This was true even for the occipital late components On the other hand, slgmficant trends over s h m u l u s position did appear for the c o m p l e x nonlingulstlc stimuh. This result may reflect the c o m p l e x i t y rather than the nonhngulstlc nature of the stlmuh It must be n o t e d , however, that there were several nonsignificant trends ( 0 . 0 5 > p < 0 10) in the P3 c o m p o n e n t for b o t h stimulus position and electrode site With a larger sample size and m o r e stimulus presentations, several of these m a y b e c o m e significant F o r each stimulus pair, 5 F-tests were p e r f o r m e d on early and late c o m p o n e n t a m p h t u d e s , producing 90 total tests With such a large n u m b e r of tests, several comparisons might reach significance by chance. T w e n t y - o n e of our F-tests reached significance, including 12 at the 0.05 level, 7 at the 0.01 level and 2 at the 0.001 level. This n u m b e r is above chance e x p e c t a t i o n , and the significant results were in the predicted direction Our design i n c o r p o r a t e d predictable s h m u l u s changes, in that for each trial, subjects knew at what poslt~on the generalization stimulus would appear. It is possible that differential preparation or arousal affected the results, since after one sequence in a particular block, subjects would k n o w what the generalization stimulus was and could
prepare for it. F o r example, a recent study [28] showed that increased arousal, as indexed by a c o n t i n g e n t negative variation and an increased evoked potential, o c c u r r e d when relevant s t l m u h were m a d e predictable. On the o t h e r hand, we did find significant differences b e t w e e n responses at different scalp locations to the same stimulus pairs, which are n o t likely to be attributable to differences in arousal. The E R P changes to the bright/dim and d i m / b r i g h t flashes have relevance to accounts of intensity generallzatlon of habituation A c c o r d i n g to a dual-process theory of h a b i t u a t i o n [ 9 , 2 6 ] , a generahzation sttmulus of different intensity f r o m the h a b i t u a t i o n stimulus would produce different a m o u n t s of generalization depending on whether it was of higher or lower intensity than the h a b i t u a t i o n stimulus. The a m o u n t of generahzation was postulated to be a f u n c t i o n of the degree of overlap of excitation an the neural elements activated by the stimuh [ 2 4 ] . Therefore, increased intensity following h a b i t u a t i o n would yield a greater response because more elements would be activated; decreased intensity w o u l d yield either a small increase in response, no change, or a decrease, depending on specific e x p e r i m e n t a l parameters [ 2 6 ] . In the present study, early c o m p o n e n t s to the dim/bright flashes showed large amphrude increments to the bright flash at all electrode sites. Conversely, early c o m p o n e n t s to the bright/dim flashes recovered in amplitude to the dim flash only at the occipital p l a c e m e n t , showing little change at either frontal or t e m p o r o p a n e t a l placements These results support the dual-process theory, rather than theories predicting symmetrical changes in response to intensity differences [21]
REFERENCES 1. Butler, R.A. Effect of changes in stimulus frequency and intensity on habituation of the human vertex potential. J acoust. Soc. Am 4: 945-950, 1968. 2. Butler, R. A., M. Spreng and W. D. Keldel. Stimulus repetition rate factors which influence the auditory evoked potential. Psychophystology 5: 665-672, 1969. 3. CaUaway, E., III. Habituation of averaged evoked potentials in man. In Habituatton, Vol II, Physiologwal Substrates, edited by H V. S Peeke and M J Herz. New York: Academic Press, 1973, pp. 153-174. 4. Davis, H., T. Mast, N Yoshle and S. Zerhn. The slow response of the human cortex to auditory stlmuh: Recovery process. Electroenceph chn Neurophyszol 21: 105-113, 1966. 5 Dlmond, S. J and J . G Beaumont (Eds.). Hemtsphere Functzon m the Human Brain New York. Halsted Press, 1974. 6. Dixon, W.J Btomedwal Computer Programs. Berkeley' University of California Press, 1975 7. Fruhstorfer, H Habituation and dlshabituatlon of the human vertex response. Electroenceph chn Neurophystol 30: 306-312, 1971. 8 Fruhstorfer, H , P. Soven and T. Jarvflehto Short-term habituation of the auditory evoked response m man. Electroenceph chn Neurophystol 28: 153-161, 1970 9. Groves, P.M. and R . F . Thompson. Habituation" A dual process theory Psychol. Rev. 77: 419-450, 1970. 10. Jasper, H.H. The ten-twenty electrode system of the raternational federation. Electroenceph clin. Neurophyslol 10: 371-375, 1958. 11 Johnston, V S and G.L. Chesny Electrophysiological correlates of meaning. Science 186: 944-946, 1974. 12 Maclean, V., A. Ohman and M. Lader Effects of attention, activation and stimulus regularity on short-term habituation of the averaged evoked potential. Blol Psychol. 3: 57-69, 1975.
13 14. 15.
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21 22.
Morrell, L. K. and J. G. Salamy Hemispheric asymmetry of electrocortical responses to speech stlmuh. Scwnce 174: 164-166, 1971. Ohman, A. and M. Lader. Selective attention and "habituation" of the auditory averaged evoked response m humans. Physiol. Behav 8: 79-85, 1972. Ohman, A., V. Maclean and M. Lader. Concomitant short-term changes in the auditory evoked response, the EEG, and reaction-time performance m relation to the temporal parameters of stimulation. Scand J Psychol 16: 177-183, 1975. Peeke, H V. S. and M J. Herz. Habttuation, Vol. 1, Behavioral Studies, Vol. II, Physiologwal Substrates. New York' Academic Press, 1973. Regan, D Evoked Potenttals m Psychology, Sensory Phystology and Chnical Medwme. London: Chapman and Hall, 1972 Rltter, W, H. G. Vaughan, Jr. and L. D. Costa Orienting and habituation to auditory stimuli: A study of short term changes m average evoked responses. Electroenceph chn. Neurophysiol. 25: 550-556, 1968. Rltter, W. and H. G. Vaughan, Jr Averaged evoked responses m vigilance and discrimination" A reassessment Sctence 164: 326-328, 1969 Schandry, R , N. Blrbaumer and W Lutzenberger. Analys~s of habituation of the components of the auditory evoked potential to stlmuh of different intensities. Psychophysiology 14: 105-106, 1977 Sokolov, Y. N. Perceptton and the Conditioned Reflex New York MacMdlan, 1963. Sutton, S The specification of psychological variables m an average evoked potential experiment In Average Evoked Potentials Methods, Results and Evaluations, edited by E Donchm and D B Llndsley Washington, D C NASA, 1969, pp 237-298.
22
23.
24
25
26
M t ~ ; F I _ A , T[-'~ I F R
Teyler, T J , R A Roemer and R t T h o m p s o n Habituation o f the pyramidal response in unanesthetJzed cat Phv~tol Behav 8 : 2 0 1 205, 1972 T h o m p s o n , R F The neural basis of s n m u l u s generahzatlon In Stimulus generahzanon, edited by D I Mostotsky Stanford. Stanford University Press, 1965, pp 154 178. T h o m p s o n , R I and W A Spencer. Habituation. A model p h e n o m e n o n for the study of neuronal substrates ot behavior Psychol. Rev 7 3 : 1 6 43, 1966 T h o m p s o n , R. F , P M. Groves, T J. Teyler and R A Roemer A dual-process theory o f h a b l t u a n o n Theory and behavmr In, Habttuatton. Vol I, Behavioral Studies, edited by H V S Peeke and M J Herz New York Academmc Pre~s, 1973, pp 239--271
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28
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Westenberg. 1 S , (; Patge, B Golub ,rod N \1 \~.cmi~cr~: Fvoked potential decremenls m aud~tor~, ~.(~e\ I l h ~ r ¢ l e rlal and ~ ontlnual ~tlmulatlon IL'[(~l'~¢t()('t?( t [711 , [l~ Neuroph_rstol 4 0 : 3 3 7 355, 1976 Wdkmson, R F and S M Ashby Selectl~c ~ttlellll,,n, Lontlngent negdlwe variation and the ew~ked potential t:]l~p[ Psrchol 1 : 1 6 7 179, 1974 Wmer, B J Stattstwal Prtnclples In Expertmental D¢'~tcp~. second edlnon New "~ork McGra~-Hill, 1971