Specificity and biasing of arousal reaction habituation

SPECIFICITY A N D BIASING OF A R O U S A L R E A C T I O N H A B I T U A T I O N . 1

J. APELBAUM,M.D.," E. E. SILVA, M.D., O. FRICK, Bach. and J.P. SECUNDO, M.D. a Departamentos de Electrobiologfa y Neurobiologla, Instituto de Investigacibn de Ciencias Biol6gicas, Montevideo, Uruguay (Received for publication: Marcll 14, 1960)

I n a recent paper, Sharpless and J a s p e r (1956) described the habituation process whereby the E E G " a r o u s a l " response provoked by a eertain stimulus became abolished when the latter was repeated a large n u m b e r of times. The present experiments were designed to analyze a limited aspect of the m a t t e r : namely, the influenee, if any, exerted by habituation to one given stimulus (brief tone) upon responsiveness to similar but not identieal excitation (tones differing in their f r e q u e n e y values, front the first and f r o m eaeh other). Observations r e p o r t e d in this eommnnieation indicated that repetition of a sound until inoperant did indeed alter the reactivity of the animal to subsequent application of other tones and, in a preferential manner, facilitated habituation to pitches similar to the one applied preliminarily. 3,[ATERIAL AND METHODS

E x p e r i m e n t s were p e r f o r m e d on a total of 21 cats c a r r y i n g electrodes implanted ehronieally in somatic sensory cortex and, occasionally, in acoustic cortex, visual cortex, basolateral amygdaloid complex, meseneephalic reticular formation, mesencephalie central g r a y matter, septum or eaudate nucleus. Types of electrodes have been described elsewhere (Segundo, Roig and ,qommer-Smith 1959); deep placements were checked histologically. A f t e r recovery f r o m i m p l a n t a t i o n I Supported in part by grants from Rockefeller :Foundalion (58122) and U S A F Office of Scientific l~eseareh (Contract No. AN 49 (638) 585). An abstract by Apelbaum, J., Silva, E. E. and Frick, (). was included in " A b s t r a c t s of Communications" X X I International Congress of Pl~ysiologieal Sciences, Buenos Aires, 9-15 August 1959, p. 18. 2 ¥ i s i t i n g investigator from I n s t i t u t e Naeional de Mierobiologia, Buenos Aires, Argentina. 3 P r e s e n t address: B r a i n Research Institute, UCLA, California, U.S.A.

effects, eats were studied daily in sessions lasting up to 6 hours. Observations were carried out in a relatively sound-proof room where animals could be observed (without seeing the investigator) and their E E G was reeorded on a Grass I I I D machine. Tones were generated by a Hewlett P a c k a r d 200 A B audio-oscillator connected to a 4 im,h Goodm a n loudspeaker placed inside the conditioning box of 55 x 45 x 35 era. W i t h this set-up, sound intensities (measured with a microphone and Sound Level Meter T y p e 1551 from Radio Co., Cambridge, 5lass., U.S.A.) varied, with the f r e q u e n c y of the tone and with the position inside the eage, within the I)2 db ±: 12 range. D u r i n g sessions t h r o u g h o u t the entire observatiou period the main group of 12 eats received tones exhibiting a frequency of 200 c/sec., a wduc fixed a r b i t r a r i l y within ~he feline range of audibility; eae.h one of these " b a s i c " tones had a duration of 5 see.; " b a s i c ' ' tones were separated from each other by silent intervals also lasting 5 see. T r a i n i n g proceeded in two stages. Stag~' I ( " P r i m a r y " habituations). " B a s i c " , 200 c/see, tones were applied in the m a n n e r deseribed above until " p r i m a r y " habituation ensued. Animals were considered sufficiently habituated when, in the course of s u c c e s s i v e s e s s i o n s , " b a s i c " to,los w e r e t!(illsistently unable to prow)ke behavioral alerting or E E G " a r o u s a l " (except p e r h a p s for minor effects in response to first few tones of session). No other tones were used durin~ this period. Stage: II ("Necmularg" habituation). The " b a s i c " 200 e/see, sound eontinued to be applied according to the same routine. I n t e r m i t tently, however, and at i r r e g u l a r intervals, single " b a s i c " tones were substituted by single 829 ]

830

J. A P E L B A U M , E. E. S I L V A , O. F R I C K a n d J. P. S E G U N D O

" t e s t " tones having the same duration (5 see.) but exhibiting frequencies of 202, 205, 210, 220, 230, 250, 300, 350, 400, 450 or 500 c/see. " T e s t " tones were systematically applied against a standard E E G background of

spindles separated by periods of relatively rapid activity (fig. 1, 2, 4) ; depending mainty on the rapidity with which cats returned to the selected control pattern, intervals between successive " t e s t " tones wtried fr()ln a few seconds to many minutes; in each session inter-trial intervals shortened as more tones were applied (Sharpless and J a s p e r 1956). Thus intercalated within the " b a s i c " sequence, the different " t e s t " tones were presented one at a time until a first " s e r i e s " (group comprising one " t e s t " tone of each frequency) was coxnpleted; thereafter and in the same fashion, successive " s e r i e s " were ap-

plied until eventually reactivity to all tones was abolished (5-95 series, at 3-15 pet" session, were presented to each animal). The order of presentation of the different " t e s t " tones of each series was randomly determined. The presence or absence of behavioral alerting and of E E ( I " a t msal' ("desynchronization", " a c t i v a t i o n " etc.) was noted after application of each " t e s t " tone. Three comph, m e n t a r y groups of (,xperiments were I)erformed. (i) Uniform intensity group. A procedure similar to the one described was followed in the :/ eats con,prised in this group but, in addition, the output of the andio-oseillator was adjusted for each " t e s t " tone according to the frequen(.y of the tone and to the situation of the animal so that intensity variations were reduced to under ÷ 3 db. The purpose of this group was an evaluation of the possible significance of intensity variations in the determination of results encountered. (it) No basic tone group. In 3 animals, successiw~ series of " t e s t " tones identical to those utilized in the main group (frequencies,

to this group informed as to tire natural evolution of habituation to " t e s t " tones, as oe(.urring ill the absence of " p r i m a r y " al)plication of " b a s i c " tones. (iii) 300 c/sec, grm~p Instead of the ~:urrent 200 c/'sec, a "basic." fre{tuen(~y of :/0() ~' se(:. was used for " ' p r i m a r y " habituatioll iu 3 other eats; during stage [[, " s e c o n d a r y " habituation was established and evaluated with " t e s t " frequencies of 2()0, 250, 270. 285, 295, 305. 315, 330, 350. 400, 450 anti 500 e set,. tither details, (tone duration, intor-tone interwds, frequency sequem'e. I)a(.kgroun(l EEG, etc.) of the experimental rm~tine wcr, identical |o those des(,ribed for the main group. This group was planned iu order to estat)lish the relationship, if any, between the flitch of the " b a s i c " tone and the reactivity patterns observed during " s e , , ( m d a r y " habitual ion. RESUI~TS Except for rapidly att(muated investigative movements in response to early " t ) a s i c " tones of stage [ and 1)erhaps to early " t e s t " tones of stage [I, behavioral eff,cts were pra,tieally absent and shall be omitted from th,' following considerations; descriptions will therefore involve ('le(~lrogral)hic asl),ets ex~dusively, obs(q'ved in somatic sensory ,ortex mdess otherwise state(l. The presence ()r al)sence of E E G " a r < m s a l " was in fact lh(, m'itieal issue ewduated after api)lieation of each "test"

S(Hllld. 1

202, 205, 210, 220, 230, 250, 300, 350. 400,

The process of " p r i m a r y " habilualion h) /he " b a s i c " it)no of 200 c see., as observed in the main group of exp(q'iments, exhibited th, same general features described in detail by Rharph'ss and .Iasper (1956). AI lhe eml of' stage I (" prinnlry' ' habitual iml ) and throughout sta~e I1 " s e ~ ' o n d a r v " habitualion). " t ) a s i c " tones of 200 e 'soe. were uuable to 1)roduee E E ( I " a c t i v a t i o n " (fig. 1, 2 ) ; " t e s t " tones applied during stage II, on the other hand, wore either ef%,tive ("I)ositive", marked white in figure 4 aml 5) or

450, 500 c/see.; durations, 5 set'. ; inter-tone intervals, variable; sequence, random) were applied in a siinilar manner. The differential eharacteristi(, of this group was that no " b a s i c " frequency was presented, either previously or simultaneously. Results pertaining

1 ' ~D e s y n c h r o n i z a t i o n ' ' e f f e c t s 1.'odm'ed 1)v ~ ' t e s t " tones, were u s u a l l y b r i e f and eomp'lr:dde to t h e ~ ' p h a s i e " type described by others (Caspers, Lerche a n d Griiter 1958; S h a r p l e s s :rod J a s p e r 1956!. N o t a b l e exceptions were provided by first tones of c o m p l e m e n t a r y g r o u p (ii) t h a t provok(~d l . ' o h m g e d effects.

AROUSAL

HABITUATION

ineffective ( " n e g a t i v e " , marked black in fig. 4 and 5). The distribution of " p o s i t i v e " and "nega t i v e " " t e s t " sounds adopted a characteristic pattern (fig. 1, 2, 4-~, 5-M): within each series, eats reacted by E E G " a r o u s a l " to frequencies that were far from the " b a s i c " value upon the pitch continuum; eontrastingly, they did not respond to those close to DIS(;RIMINATION IN

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,'5;7., Fig. 1 EFFECTS OF "TEST" T O N E S I N F I R S T SERIES. SPECIFICITY O F " P R I M A R Y '~ H A B I T UArI)N. I n f i g u r e s 1, 2, a n d 3 E E G records p e r t a i n to s o m a t i c s e n s o r y cortex, c a l i b r a t i o n s rep r e s e n t 1 see. a n d 50 ~V. a n d values on left of each t r a c i n g allude to f r e q u e n c y of " t e s t " tones utilized ( a p p l i c a t i o n is i n d i c a t e d in each ease b y a thick horizontal bar underneath the record). After "primary" h a b i t u a t i o n to 200 e/see., t e s t i n g in f i r s t series i n d i c a t e d t h a t t h e " b a s i c '~ (200 c / s e e . ) a n d n e i g h b o u r i n g (202, 205) t o n e s were i n o p e r a n t b u t " b o r d e r - l i n e " (210) a n d r e m a i n i n g v a l u e s (220, ....... , 500) were effective.

200 c/see.

The tone capable of producing and nearest to the " b a s i c " sound in terms of frequency value marked, for each cat and each series, the separation between inefficacy and efficacy and will be referred to as " b o r d e r - l i n e " tone (e. g., 210 c/see, in fig. 1, 500 c/see, in series 27 of fig. 2) : tones with frequencies between "basil," and " b o r d e r - l i n e " values were in-

"desynchronization"

831

operant; beyond the " b o r d e r - l i n e " tones were operant (fig. 1, 2, 4 M, 5 5I). In the first series, " b o r d e r - l i n e " tones were encountered at 205 (1 eat), 210 (2 eats), 220 (5 eats), 230 (1 cat) and 300 c/see. (2 cats); the remaining animal was completely unresponsive ( " t e s t " tones were all ineffectual) (fig. 1, 2, 4-M, 5-M).1 As series were repeated, reactivity of each animal dccreased g'radually and total habituation to all " t e s l " tones ensued eventually (fig. 2, 5-5I). The process whereby non-responsiveness bec~ame generalized followed a typical patlcrn characterized by the fact that, in successive series, the " b o r d e r - l i n e " tone moved gra(tually away from the " b a s i c " frequency (200 e / s e e . ) ; finally, inefficacy implicated ev('n the extreme value tested (500 c se~.) (fig. 2. 5-M). Fig'ure 2 shows representative st(~ps in the evolution of " s e c o n d a r y " habituation in one animal in which, before total indifferem'e was achieved (series 34) the "t)order-lim~" inoved from its initial location at 210 (series 1) through 250 (series 4), 300 (series ]1) and 5{){le see. (series 27). (~ompletion of' the process required from 2 to !}5 series and 2-10 days but, since series and sessions were not distributed in a standard fashion in different animals, values were not strictly coml>arabh'. There was, in addition, a degree of individual, variability: certain preparations (e.g., tame eats) showed quickly and after a shm't tmmber of series, a markedly reduced degree of responsiveness, reacting to few if any tones; others (e.g., savage eats) continued to be r~'active throughout many series. The final status of comph'te habituation (or non-responsiveness to all " t e s t " tones) was achieved basically by way of the characteristie process described abow ~. Minor deviations from the typical pattern occurred, however, and assumed two main types. (a) I/eappearance of responsiveness to some of the tones previously rendered inoperant was observed c u r r e n t l y at the beginning of each daily session (e.~. : fi~. 3; series 1 A r e f r a c t o r i n e s s similar to t h a t of this app a r e n t l y h e a l t h y a n i m a l w a s e n c o u n t e r e d also i n : (1) a n u m b e r of oi~viously sick (e.g., i n f e c t e d , epileptic, etc.) e a t s ; (it) a p r e l i m i n a r y series of r a b b i t s tested u n d e r a n i m a l h y p n o s i s (Silva, E s t a b l e a n d S e g u n d o

1959).

832

J. A P E L B A U M , E. E. SILVA, O. F R I C K :~n(l J. P. SEGUNDO

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3 and 4 of eat representing group i in fig. 5) or, during sessions, after prolonged intervals in which tones had been omitted; recovery of efficiency involved frequencies close to the " b o r d e r - l i n e " and few series were then neeessary to re-establish the original level. This " d e - h a b i t u a t i o n " was remindful of the phe-

833

Table I was constructed by way of summ a r y and showed, for each " t e s t " frequency, the percentage of effective presentations in total mm~ber of applications, in all eats and all series. Values were low for tones close 1o the " b a s i c " sound upon the fre
DE- HABITUATION S.68

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DE H A B I T U A T I O N . When in the course of " s e c o n d a r y " habituation " t e s t " tones were not applied during a period of hours, exploration after that interval showed that some previously negative values recovered efficacy: recuperation involved tones close to the " b o r d e r - l i n e " wtlue. In series 68 ($68) applied on March 27, 1959, " t e s t " tones of 230, 300 and 450 e/see, were inoperant; in the following series ($69) applied the following d:ly (March 28, 1959), 300 and 450 (but not 230) hec'mm effective.

nomenon described by Hern~ndez Pe6n, Scherrer and Jouvet (1957). (b) 1-2 non-effective values were commonly encountered within the range of effeetiw, tones (e.g., 230 e/see, in eat 8 of fig. 3 ) ; this irregularity usually became more notieeable as the number of applied series increased.

increased progressively for intermediate values as they moved away from 200 c/see. (e.g., 5.8 per cent for 205, 6.4 per cent for 210, • . . , 56.1 per cent for 450) and reached a maximum for the highest t)itch of all (e.g., 64.q per cent for 500 e/see.). This si~znificant relationship that existed for each " t e s t " value between effeetiveness and frequency

Fig. 2 E F F E C T S OF " T E S T " TONES I N SUCCESSIVE SERIES. B I A S I N G OF " S E C O N D A R Y " H A B I T U A T I O N . The " b a s i c " (200 c/sec.) tone was inoperant. As successive series were applied in the course of " s e c o n d a r y " habituation, the " b o r d e r - l i n e " tone (separating negative from positive pitches) passed from its initial vnlue at 211, (series 1) through 250 (series 4), 300 (series 11) and 500 c/see. (series 27); eventually. total ineffectiveness was achieved (series 34). S M C somatic sensory cortex.

834

J. A P E L B A U M , E. E. S I L V A , O. F R I C K a n d J. P. S E G U N D O

separation f r o m the " b a s i c " tone subsisted even though both the n a t u r a l evolution towards non-responsiveness as habituation advanced and the presence of irregularities (a) and (b) tended to attenuate discrepancies.

Complementary Groups. (i) Uniform intensity group.

W h e n the oscillator output was adjusted according to frequency of tone and position of auimal so that intensities received by the latter were TABLE

eat to another, changed considerably; their total n u m b e r per series increased more or less regularly. F i n a l l y and by series 11-12, complete i n o p e r a n c y was achieved (fig'. 4-I[, 5 - I I ) . This i r r e g u l a r consmmnation of "seco n d a r y " indifference in animals not subjected to " p r i m a r y " habituation contrasted with the orderliness of results observed in groups main and i submitted to " b a s t ( . " tones : the I)resence of such a m)torions difference

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uniform, responsiveness to first and subsequent series followed an evolution identical to that described of cats in m a i n group (fig. 4-[, 5-I). This similarity indicated t h a t intensity variations were not significant in the determination of "secondary" habituation patterns. (it) "No basic" tone group. Animals included in this g r o u p went through a first period of 2-4 series in which all "test" tones were effective. I n a second period involving series 3-11, certain tones were i n o p e r a u t : t h e y did not necessarily exhibit close f r e q u e n c y values and, in succeeding series or f r o m one

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Fig. 4 EFFECTS OF "TEST" T O N E S I N F I R S T SERIES. SPECIFICITY OF "PRIMARY" HABITUATION IN DIFFERENT GROUPS. Each large r e c t a n g l e includes f i r s t series of cats wittdn one g r o u p . H o r i z o n t a l or vcrtical n u m b e r sequences i m dicate respectively d i f f e r e n t p r e p . n ' a t i o n s w i t h i n one g r o u p (e.g.; 1, ........., 12) or d i f f e r e n t test frequencies a p p l i e d to each p r e p a r a t i o n (e.g., 202, ..... , 500). W t m n p r e c e d e d b y "primary" h a b i t u a t i o n ( g r o u p s M. I, I I I ) , t h e f i r s t " t e s t " series i n d i c a t e d t h a t t o n e s close to t h e " b a s i c " s o u n d (200 c/see. ill g r o u p s h{ a n d I ; 300 c/see, iu g r o u p I l l ) were i n o p e r a n t a n d t o n e s removed, o p e r a n t . W h e n n o t preceded by p r i m a r y h a b i t m t t i o n ( g r o u p I [ ) all t o n e s were positive. I n f i g u r e s 4 a n d 5, t o n e s with positive, n e g a t i v e or d o u b t f u l e f f e c t s are r e p r e s e n t e d respectively w i t h white squares, black s q u a r e s or question m a r k s ; tones n o t t e s t e d with short, horizontal black ]ines. D O U B T . , d o u b t f u l , NO R E S P . , no res p o n s e ; N O T T E S T . , n o t tested, R E S P . , response.

AROUSAL HABITUATION demonstrated that "secondary" habituation p a t t e r n s of the l a t t e r g r o u p s d i d n o t e m a n a t e f r o m a n i n b o r n r e a c t i v e m o d a l i t y c o m m o n to all i n d i v i d u a l s of the species b u t , on the eont r a r y , were a consequence of the p r e l i m i n a r y t r a i n i n g r o u t i n e c o n s i s t i n g i n r e p e t i t i o n of the " b a s i c " tone a n d l e a d i n g to " p r i m a r y " habituation. (iii) " B a s i c " tone 300 c/sec. After " p r i m a r y " h a b i t u a t i o n to 300 c/see., n o n - e f fective " t e s t " tones were also g r o u p e d t y p i c a l l y : a c c u m u l a t i o n o c c u r r e d however a r o u n d the ~ew " b a s i c " v a l u e a n d n o t a r o u n d 200 e'sec, as in the m a i n g r o u p . I n the f i r s t series t h e y were f o u n d w i t h i n the f o l l o w i n g i n t e r v a l s ( i d e n t i f i e d b y the respective " b o f d o t - l i n e " tones) : 285-305 (1 c a t ) , 295-31.5 (1 e a t ) , 285-330 c/see. (1 cat) (fig. 4 - I l I ) . Thereafter, " b o r d e r - l i n e " v a l u e s m o v e d g r a d u a l l y a w a y f r o m 300 c//sec, t o w a r d s tile deeper s o u n d s on one side a n d the h i g h e r s o u n d s on the o t h e r ) F i n a l l y , complete " s e c o n d a r y " h a b i t u a t i o n was e o m p l e t e d (fig. 5 - I I I ) . These results showed t h a t the n o n - e f f e c t i v e freq u e n c y r a n g e p r o v o k e d b y " p r i m a r y " habit u a t i o n did n o t n e c e s s a r i l y i n v o l v e the 2002:~0 ('/see. i n t e r v a l in all c a t s : on the cont r a r y , it could v a r y f r o m one ease to a n o t h e r and, for eaeh a n i m a l , was located in the v i c i n i t y of the precise " b a s i c " v a l u e to which it was i>reviously a n d s i m u l t a n e o u s l y submitred. I n all groups, the b a e k g r o n n d E E G was a critical issue in the d e t e r m i n a t i o n of resp<)nsiveness: w h e n p a t t e r n s i n v o l v e d g r e a t e r a m o u n t s of slow a c t i v i t y ( a n d p r o b a b l y indicated g'reater deg'rees of r e l a x a t i o n ) , the t a n g o of n o n - e f f e e t i v e n e s s a u g l n e n t e d m a r kedly, u s u a l l y at the expense of " b o r d e r l i n e ' " a n d n e i g h b o u r i n g values. This r e a s o n s u p p o r t e d the r e q u i r e m e n t t h a t " t e s t " s o u n d s should be a p p l i e d a g a i n s t a s t a n d a r d backg r o u n d (fig. 1, 2, 3). Records f r o m a u d i t o r y or v i s u a l cortex, head <>f e a u d a t e n u c l e u s , b a s o l a t e r a l a m y g dala, s e p t u m , m e s e n e e p h a l i c r e t i c u l a r f o r m a In certain preparations pertaining to the mnin group (primarily habituated to 200 e/see.) extra " t e s t " tones of 195 e/see, were ineffective. This suggested that, also after habituation to 200 c/see., non-effectiveness occurred on both sides of the ' ' basic ' ' frequency.

835

tion and mesencephalie central gray matter, i n d i c a t e d t h a t i n g e n e r a l these areas r e a c t e d to tone a p p l i c a t i o n i n the same f a s h i o n as tile more w i d e l y tested somatic s e n s o r y , o r t e x ( S h a r p l e s s a n d J a s p e r 1956). I n one a n i m a l , however, the a u d i t o r y cortex was s o m e w h a t M ' B A S I C " TONE 200".,

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Fig. 5 EFFECTS OF " T E S T " TONES IN SVC(YESSIVE SERIES. BIASING OF "SECONI)ARY" tIABITUATION IN DIFFERENT GROUPS. Each large rectangle derived front a representntive eat of each group. Horizont'd or vertienl iiill)ll)er se(tuellees iIldieate respectively successive series (e.g., 1, , 11) or different " t e s t " frequencies applied (e.g., 2(~2, ........ , 500). When preceded by "primary" hal)itu'~tion, "secondary" habituation was est:d)lished in a typically biased fashion (Groups M, i, iii). Noneffectiveness of tones close to the " l m s i e " v;due (200 e/see, in groups M and i; :~00 c/see, iu group iii) was favored and they either were initially inoperant or l)ee:~me so on a typical se(lu(mee. [n group i, applied tone intensitios were uniform. When not preceded 1)y " p r i m a r y " lmbituation, ' ' seem,la r y " habituation w:(s established in a r'~ndom f:lshion group it).

more reactive t h a n the rostral area a n d E E G " a r o u s a l " in the f o r m e r was occasionally p r e s e n t w i t h o u t e o n c o m i t a n l ehano'es in the l a t t e r : e x p l o r a t i o n of the p r i m a r y au(tih)ry p a t h w a y is now i n progress. DISCUSSION The E E G " a c t i v a t i n g " c a p a c i t y of successive series of " t e s t " tones was e x p l o r e d i n cats a c c u s t o m e d to a " b a s i c " p i t c h : if r e s u l t s

836

J. APELBAUM, E. E. SILVA, O. FRICK and J. P. SEGUNI)()

ed that as a result of "primary" habituation the audible continuum of the cat had been separated into three main regions. (a) A in separate regions of the diagram (fig. 4, 5). central negative segment contaitled the " b a Distribution indicated that for each l)repara- s i c " frequency and extended a limited distion, the ability of each " t e s t " tone to induce tance on both sides ( " b o r d e r - l i n e " t(mes were E E G " a r o u s a l " in somatic sensory cortex de- . o t included therein). Api)arently, the propended upon two critical issues: (i) mmlber tess that neutralized the " b a s i c " lone was of times the " t e s t " tone had been presented: generalized partially an(l, as a (,(msequence, eOml)arison of the same frequency in suc- inefficacy was imI>ressed also on this interval: cessive series showed that values positive in terms of eal)acity to ew)ke E E G "' arousal", when novel lost effectiveness as they became such frequencies were no different from the familiar. This illustrated production of " b a s i c " value. (b) Two lateral positive rehabitv.ation by repetition; having been an- gi(ms eoml)rised the rest of the audible i'at,~e, alyzef positive learnt(mes in first series; 2, effects of " t e s t " tones ing (Neff and I)iamond 1.q5~). (%nsequently, in sueeessiw~ series) of the main fin(ling de- neural mechanisms mediating E E G "' a r o u s a l " fined above shall concern the following dis- showe(t a sm'prisingly acute capaeily to dis,mssion: each reflected a general feature (1, criminate between (lifferenl pitches) specificity; 2, biasing of subsequent habfluatimls) of the process of habituation and both 1 In these exl)erinmnts, the specificity degree of justified considerations referrin~ to possible '~primary" hal)itu,qtion was ol)viously rel:~ted to the background EEG activity:: namely, slower (faster) ]lle(,halliSlllS. patterns were associated with lessened (enhanced) (1) Effec~s of "test" tones in first series. frequency discerning abilities amt greater (lesser) Specificity (of "primary" habituation). degrees of generalization. This correlation observed also by Caspers, Lerche and Griite," (195~) could [noperaney of frequencies close to the " b a s i c " explain an apparent contradiction betwcen lhe ",Itsvalue contrasted with operancy of those be- criminating" eqpacities f
were then plotted as function of series number and fre'lueney value, positive and negative effects aeemmflated selectively with-

AROUSAL HABITUATION (2) Effects o[ " t e s t " tones in successive series. Biasing (of " secondarg" habituatbm ). A s y m m e t r y of the biased " s e c o n d a r y "

h a b i t u a t i o n derived, not only from initial n e g a t i v i t y of tones ill central region (a), but also from the fact t h a t fre:lueneies ilmluded ill lateral regions (b), t h o u g h u n i f o r m l y l)OSitive ml their first presentation, were not e:tuivalent as to their ability to remain efft'etive in the course of successive applicatim]s. Initially effeetiw, tones did not becmue ne~zative s i m u l t a n e o u s l y t>r r a n d o m l y but sm'eundled ttl repetititm in a characteristic seqUell~.e sug'gestiug: firstly, that the l)ro,'es~ t h a i neutralized the " a r o u s i n g " ' ability of " b a s l e " and, hy generalization, adjm.ent sttumls also hilnlered " a c t i v a t i o n " ttl tither tom's; set.ondly t h a t refractoriness adtlpted a typical dislribution u p o n the pitch eontimmnl, a t t e n u a t i n g as f r e q u e n c y separation from " h a s t e " t o n e int~reased ( m a r k e d for central tones, it bloel~ed " a r o u s a l " It) first l)resentation; prog'ressively less intense for others, it r e q u i r e d the additional eaneelling effet.t of l a r g e r mmfllers of applieations). Biasing of " s e e o n t t a r y " by " p r i m a r y " habiluatiou essentially indieated thai learuin~' not to react to ¢,ertain sounds was favilitalt,d by having' first learned not to reslmnd to a similar " b a s i c " frequency. A c u r r e n t notit>n t.laims that a c q u i r e m e n t of one ability will ~,xpedite subsequent a t t a i n m e n t of skills alike Ill the first and experiments described ahoy,, SUl~ptlrted the applieabilitv tit the general t.tmtentiotl to this special ease of nt,~'ative h,aruiug. The distribution of refractoriness prow)ke, I by " p r i m a r y " h a b i t u a t i o n wa'~ related critically ttl tile linear a r r a n g e m e n t of tone fr(','lut'ut'y values u p o n the pitch e o n t i n u u m . (!oin,ddeuee between non-responsiveness a n d pit(,h position p a t t e r n s seems possible only if habituatiotl impresses itself upon a strut'ture in which the linear tone f r e ' l u e n c y scale were repr,sented by a p a r a m e t e r exhibiting a similar linear a r r a n g e m e n t . Aecordill~' to by other investigators during deep sleep. Under such delwessed conditions, (i) eats habituated to 500 e/see, were indifferent also to 600 e/see., :rod (it) eats trained to respond to 200 e/see, were "aroused '~ qlso by 250 e/see. (Segun(lo, Roig and SonnnerSmith 1959; Sharpless and Jasper 1956).

$37

available descriptions, such parallelism may be achieved, within the nervous system, by spatial a n d / o r t e m p o r a l p a t t e r n s of m.tivity (Galambos 1!)53; Galanlbos anti I)avis 1943); one nlay ~'onjecture that it is within the fum.tional possibilities tlf both operational modes to s u f f e r changes h,adino' to a habituated rendition exhibiting eharat.hwistie distribulion. In a ttnmtoph, mechanism, il~ which different l)itche~ evoke maximal activity in spatially different areas and linearity issues fronl sequential arrallgelllellt of areas m.~,ordill~' l o tone frequem,y valut,s, habituatiml ~.ouht be a~so~'iated witll refractoriness al ihe proje~'tirol site of the repeated tml,,: su,.h a t'o¢.us eouhl invade atljaeent regious dm'rmnenlally and p r e f e r e n t i a l l y rethlee et't'e<'tiveness of related l o n e frequem'ies. ~ In a ~'mlvt,r~en~'e mechalfiSln, in which ttifferel,t Ifil¢.hes evoke d i f f e r e n t temporal p a t t e r n s of dist.har~'¢, in the sanle g r o u p tlf IlellCOlleS ~tlltl lim,arity isslles l'ronl the emltinuons variation of parameters (e.g., interspike inierval) itlenlit'ying' discharge correspondin-' ttl ,.m,h llit(.h, hattituation ~.ould be associated with s~qe,.live refractoriness of seetmd order neurones to lhe p a t t e r n belonging to the rt'lwaie:l lone: Im'k of sns(.eptibility (.ould imldieate similar discharges d e c r e m e n t a l l y and i hus l!T'eferenl tally r e f l l l ( ' e e f f i c a c y tlf related lone freqm'm'ies. A p a r t frt)m these h y p o t h e l i r a l ~'onsideralimls t,om,erlfing the potetliial ability ot' ('('rlaiu functional p a t t e r n s to a e ( , o l t / i ) a l l v t)i" ('Veil tletermine habituation, it does tltll s e e m periiilellt It) e l a b o r a t e here ut)tlll other aslleets of its g'em, sis, as locus or basle nle~'hanisms t'm" instant,e; evidence reg'ardiu~z these proldt,ms is either insufficient or ~'onflieiinu' and fm,ls disehlsed in this paper did ntll shed f u r t h e r li~'ht upon them (Herniln~h,z-I'edn. .Imwet and S e h e r r e r 1957; RoiR' and S~tmnl~,r-Smith 1959: Sharpless and ,Iaspt,r 1956i. All i m p o r t a n t lmrti(,illation of h,arned issues in 1)rt)dnt,tioll of aelivaliml p a t t e r n s svch as the arousal, alertin~z and slarih, reactions has been d e m o n s t r a t e d t,xlwrinuultally and m a y lead to t,ither loss (habiiuatiou'~ or ae~.Onil)lishment (eonditioniu~') of tlw dif-

1 This hypothesis is remindful of Pavlov's opinion as to distribution of eorfi¢.al excitation or inhitdtion (Konorski 19473.

838

ferent

J. APELBAUM, E. E. SILVA, O. FRICK and J. P. SEGUNI)O

responses

under

precise

conditions

(Caspers, Lerehe a n d Griiter 1958; Roig a n d S o m m e r - S m i t h 1959; R o w l a n d l q 5 7 ; Seo'undo, Roig a n d S o m m e r - S m i t h 1959; Sharpless and ,Jasper 1!)56). The present observations em each other, were presented (" secondary" habituation). As a c(mse,'tuenee of having' been aeeustome(l to the " b a s i c " tone, responsiveness of cats was modified in the sense t h a t effectiveness of " t e x t " tones near the " b a s i c " value n p o n the pitch c o n t i n u u m was redueed in a sele(,tive m a n n e r . Reduction became manifest throuu'h two essential aspeets, eaeh s,g'~'esting d i f f e r e n t but e o m p l e m e n t a r y conelusions. (i) On their first presentation, sounds removed f r o m the " b a s l e " value by at least 5 e/see, in '2(10 were effeetive; those (;loser, ineffeetive. Specificity of h a b i t u a t i o n was thus limited t)y generalization of i n o p e r a n c y to frequencies a d j a c e n t to the " b a s i c " value. Notwithstan(lina' this restriction, mechanisms mediating' E G G " a r o u s a l " exhibited a relatively m a r k e d ability for d i f f e r e n t i a t i n g between dissimilar pitches. (ii) In sueeessive series, initially positive tones became ineffeetual following a stagR'ered sequence in which values closer to t h , " b a s i c " f r e q u e n c y achieved n e g a t i v i t y earlier. Henee, the process t h a t neutralized

" b a s i c " and, b y generalization, aeared related critically to the lim'ar a r r a n g e m e n t of tones upon lhe pitch scale. Rf:SUMI:: Les expOrMwes ont 6% r6alisfes sur des chats p o r t e u r s d'61ectrodes implant6s chez lesquels la r6aetivit6 6tait 6valu6e p a r la pr6sence d ' u n e c a e t i v a t i o , >> E G G g'raphiqm, au niveau du cortex somato-sensoriel. Les a n i m a u x f u r e n t tout (l'ahord somnis a l ' a p p l i e a t i o n r6p6t6e d ' u n sou <> jus!lu'h ce que celui-ci devienm' inop6rant ( h a b i t u a t i o n <

>). Puis des s6ries sueeessives de ¢ sons tests >> a y a n i des fr6quenees diff6rentes h la lois du ¢ s o n de base >> et les llllS p a r ral)l)ort allX autres, 6talent pr6sent6es jusIlu'i! ce qu'ils deviennent &'alement neutres (habituation < daire >>). t)aree que les chats avaient 6% h a b i t u & an son <> ils eurent leur r6ponse mo(lifi6e p a r les sons <> (d6viation) (t(, telle manibre que l'effieaeit6 des sons <> voisins (le la v a l e u r tonale > 6tait r6(luite de faeon sdleetiw,. La r6> 6talent (,fficaees. Ceux plus voisins 6talent imfffieaces. La sp6eifieit6 de l ' h a b i t u a t i o n 6tait ainsi limit6e p a r la g6n6ralisation de l'inop6ra.(,e pour des fr&iuenees voisines (le la valeur du son ¢ de l>ase >>. E n d6pit de cette restriction les m & a n i s m e s resl)onsables (le l'6w,il E E G gTaphique m o n t r a i e n t un l)OUvoir relativem e n t mar(tu6 D(mr la diff6reneiati(m entre (h's notes dissemblables.

839

AROUSAL H A B I T U A T I O N

(ii) Au eours des s6ries sueeessives des sons initialement positifs devinrent ineffi(.'aces en suivant une eourbe dans laquelle les valeurs les plus proehes de la fr6quenee de la tonalit6 de ¢ base >> devinrent plus rapidemenl ineffieaees. Ainsi le proeessus qui neutralisait les sons ¢ de base >> et p a r g6n6ralisation les sons voisins affeetait aussi les autres valeurs. Puis'lue l'habilit6 a rester effieaee dans le eours d ' a p plieation sneeessive a u g m e n t a i t lorsque la s6paration de la not(, p a r r a p p o r t 'h la valeur (< de base >) augmentait, les imp6diments apparaissant de fa(jon d6erementielle. Deux eharaet6ristiques de l'habituation au son ont ainsi 6% mis en 6videnee: l ' u n la sp6eifieit6, l ' a u t r e l'influenee de la succession de proeessus d ' a p p r e n t i s s a g e du m~me type. Les deux apparaissent reli6s de fa~on critique ~'~ une ligne d ' a r r a n g e m e n t des sons sur line 6ehelle tonale. ZUSAMMENFASSUNG

Bei Katzen mit implantierten E l e k t r o d e n wurden E x p e r i m e n t e ausgefiihrt, in welehen die Reaktivifiit auf G r u n d des Vorhandenseins der E E G - A k t i v i e r u n g in der somatosensorisehen Gehirnrindenzone gemessen wurde.

Die Tiere w u r d e n einem " G r u n d t o n " Reiz unterworfen, bis dieser keine bioelektrisehe Weekreaktion mehr h e r v o r r u f e n konnte ( Adaptionserseheinung). I m Gefolge der G e w 5 h m m g an den " G r u n d t o n " veriinderte sieh die Reaktivitiit der Tiere und zwar so, dass die W i r k s a m k e i t d e r " TesttSne", welehe im F r e q u e n z s p e k t r m n dem " G r u n d t o n " nahe standen, selektiv vermin(left wurde. Diese Reduktion k a n n m a n hauptsiiehlieh auf G r u n d yon zwei Tatsachen feststellen, welehe zu Sehlussfolgerungen fiihren die, obwohl gegenseitig komplementiir, u n t e r sieh vers~,hieden sin& (i) Bei der ersten Priisentierung waren Tiine, welehe yon der " G r u n d t o n f r e q u e n z " zum mindesten um 5 Hz in 200 differierten, wirksam, w:Ahrend andere, welehe der Grnndtonfrequenz niiherstanden, jedoeh u n w i r k s a m v.'are 11.

Die Spezifizit~t der GewShnung war also begrenzt dureh eine gewisse Verallgemeinerung dec Unwirksamkeit yon Frequenzen, (lie dem " G r u n d t o n w e r t " nahe standen. In aufeinanderfolgenden Serien wur(len anf:Anglieh wirksame TSne unwirksam. Dies wurde erreieht d u t c h eine ~'estaffelt alternierende Polge von Reizen, wi~hrend weleher TSne mit Frequenzwerten welehe (let '~ (~rundt o n f r e q u e n z " nahestanden, friiher ihre Wivksamkeit verloren. Demzufolge seheint es, dass dec I)rozess, weleher den " ( I r u n d t o n " und, dutch Generalisation, ihm nahestehende W e r t e neutralisierte, aueh andere Werte beinflusste. Da die F:Ahigkeit, wirksam zu bleiben, im Verlauf von aufeinanderfolgen(len I)r:,isentierungen sieh verstiirkte, wemt die Differenz yore " G r u n d t o n w e r t " sieh vergrSsserte, Mum m a n annehmen, dass der I[emmung'sprozess in abfallender Weise w)r sieh geht. Zwei Aspekte der (lewShnmlgserseheinung werdeu betont: Spezifizititt und ihr Einfluss auf Lernvorgiinge :,thnli(dler Art. Beide hfingen eng mit dec linearen A n o r d m m g dec Frequenzen auf tier Tonskala ZllSallllllell. REFERENCES CASPERS, H., IJERCHE, E. lind GRUTER, ]~. Adaptation-erscheinungen der akustiseh ausgelSstmt Weckreaktion bei Reizung mit definierteu Tonimpulsen. Pfliig. Archly. gesamte Physiol., 1958, 267: 128-141. GALA~.{BOS, R. Microeleetrode studies on medi:fl genieulate body of cat. I I I Response to pure tones. J. Neurophysiol., 1952, 15: 381-400. GALAMBOS, R. and ])AVIS, I{. The response of single auditory nerve fibers to acoustic stimulation. ,1. Neurophysiol., 1943, 6: 39-58. HERN~NDEZ-PEON, R., JOUVET, ~1. and SCHERRER, H. Auditory potentials at cochlear nucleus during acoustic habituation. Aeta Neurol. Latinoamer., 1957, 3: 144-156. HILGARD, E. R. and MARQUIS, ]). Cj. Conditionb~g and Learning. Appleton-Century-Crofts Inc., New York, 1940, X I , 1-429. KONORSKI, J. Conditioned Reflexes a~d Nenrone Organization, Cambridge University Press, 1948. NEPP, W. ]). and DIAMOND~ T. I. The neural basis of auditory discrimination. In: Biologic~d and Biochemical Bases of Behavior. The Univ. of Wisconsin Press. Edited by Harry F. tlnrlow and Clinton N. Woolsey. 1958, XI'X, .f76: 101126. RoIG, J. A. y SOSL~IER-SMITH~ J. A. Atemmcidn especifica del sobresalto provocado por exeitaeidn

840

J. A P E L B A U M , E. E. S H , V A , O. F R I C K a u d J. P. S E G U N I ) ( )

nerviosa central. A n . Fae. Med., Montevideo, 1959, 44: 410-413. [~OWLAND, V. D i f f e r e n t i a l electro e n c e p h a l o g r a p h i c response to conditioned a u d i t o r y s t i m u l i in a r o u s a l f r o m sleep. E E G Clin. Neurophy.~iol., 1957, 9: 585-594. ~EGUN1)O, J. P., ROIG~ J. A. a n d SOMMER-SMIT[{, J. A. C o n d i t i o n i n g of reticular f o r m a t i o n stimula-

tion e f f e c t s . E E G Clin. N~,¢rophy.~iol., 1959, 11: 471-484. SHARPLESS, S. alld JASPER, H. II. [[abitu:ttion of' the " a r o u s a l " re.letion. Brain, 1956, 79: 655(iS(). SlgV_~, E. E., ESTABLE, (~. fill(1 SEGI;NDI), J. P. F a r t h e r ol)servations on a n i m a l hypnosis. Arch. ital. Biol., 1959, 97: 167-177.

ITeference: APELBAUM, J., SILVA, E. E., FRICK, O. a n d SEGUNDO, J. P. Speeifi(qty a n d b i a s i n g of :lrousal reaction

habitu:Jtion.

EEG

Clb~.

,~Te~lrophysiol., 1960, 1:?: 829-840.