Behavior “attention” and fear induced by cortical stimulation in the cat

BEHAVIOR " A T T E N T I O N " A N D FEAR I N D U C E D BY CORTICAL STIMULATION IN THE CAT 1 CHRISTIAN FANGEL and BIRGER R. KAADA, M.D. Neurophysiological Laboratory at the Anatomical Institute, University o[ Oslo, Norway (Received for p u b l i c a t i o n : D e c e m b e r 24, 1959) INTRODUCTION

In a previous study, the cortical areas were nmpped from which a generalized eleclrocortical activation (desynchronization, arousal) could be evoked by electrical stimulation in the cat (Kaada and Johannessen 1!}60). These cortically induced changes in the E E G are seenfingly identical with those observed in awakening from normal sleep and drowsiness to awareness, or in alerting to attention, by peripheral sensory or brain stem reticular stimulation. Comparable behavior responses have also heen evoked by cortical stinmlation in unanesthetized animals through chronically implanted electrodes (see below), and the present study is concerned with a more exact determination of the areas y M d ing such effects in the eat. The relation of the effective zones to the areas which on stinmlation in anesthetized animals produce electroeortieal activation, inhibition of spontaneous movements, contraversion, and autonomie responses is discussed. On stinmlating circumscribed cortical zones of the medial aspect of the cat's hemisphere, Kaada, Jansen and Andersen (1952, 1953) observed a typical behavior response described as " s e a r c h i n g " or " a t t e n t i o n " . The response is similar to that previously deseribed as the " a r r e s t " reaction elicited from the anterior cingulate and p y r i f o r m cortex (Kaada 1951). In the awake animal the effect consisted of an immediate arrest of all spontaneous activity in progress, followed by glancing or searching movements of the eyes and head, usually towards the contralatcral I S p o n s o r e d in p a r t by t h e N o r w e g i a n Reseqrch Coun(.il for Science a n d t h e H u m a n i t i e s , and in p a r t b y t h e A i r Force O f f i c e of Scientific R e s e a r e h of t h e Air Research and Development Command, United S t a t e s A i r Force, t h r o u g h its E u r o p e a n Office, m~der c o n t r a c t A F 61 (514)-1127.

side. A drowsy cat could readily be aroused to alertness with a corresponding attentive facial expression. Responsive sites, among negative ones, were located throughout the entire extent of the cingulate and hippocampal gyri, the hippoeampus and the m e d i a l p r e f r o n t a l cortex. The latter region was more extensively studied by Jansen, Andersen and Kaada (1955-1956) and it was shown that the attention response was probably mediated through the thalamic midline and intralaminar nuclei. On increasing the stimuhls strength the attention response sometimes developed into reactions of anxiety and fear terminating in flight. This was particularly seen from electrode sites within the cingulate gyrus. During the preparation of the present paper, the communication by Sano (1958) became available. This author has obtained similar behavior changes, described as search-, ing, anxiety, fear and escape on s t i m u l a t i n g the lower ends of the posterior suprasylvian, ectosylvian and sylvian gyri in the cat. Segundo, Arana and French (1955), working with monkeys, have reported comparable behavior " a r o u s a l " and fear resulting from excitation of the cingulate and first, temporal gyri, temporal pole, frontal oculomotor field and the para-oceipital area. MATERIAL

AND METHODS

A total of 159 electrodes were i m p l a n t e d in 42 a d u l t c'tts. These r e p r e s e n t a n a d d i t i o n to lhe 104 medial cortical sites earlier r e p o r t e d f r o m our Labo r a t o r y ( J a n s e n , A n d e r s e n a n d K a n d a 1955-1956), m a k i n g a total of 263 electrodes ( f i g . 2). The procedure employed w a s the s a m e as t h a t described previously ( K a a d a , J a n s e n a n d A n d e r s e n 1953). I t should be e m p h a s i z e d t h a t in order to "lvoid m e n i n g e a l s t i m u l a t i o n the b i p o l a r electrodes, i n s u l a t e d except for the tips, were i n s e r t e d a b o u t I ? ram. into l h e cortex.

[ 575 ]

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C H R I S T I A N F A N G E L and B I R G E R R. K A A D A

RESULTS

( A ) The " a t t e n t i o n " response. F i g u r e 1 shows the t y p i c a l a n d f u l l y d~;veloped " a t t e n t i o n " response as induced by cortical stimulation in the conscious animal. hfitially there is an arrest of all s p o n t a n e o u s o n g o i n g activities, such as walking, licking, side-to-side movements of the tail and shiverins'. F r e q u e n t l y there is also an initial eessa-

Fig. 1 B.dmvior ":lttention" 1)roduccd by stimulation of the m~.dial frontal cortex. A. before, B. during stimulalion. tion of r e s p i r a t i o n which is usually SOOll followed by acceleration of b r e a t h i n g with diminished excursions. The a n i m a l shows signs of arousal, it becomes alert, the facial expression a n d the whole a t t i t u d e of the a n i m a l (,hange to one of attention. The cat seems bewildered and surprised. T h e n follows n~ocemerits of a ~ orienting character. I t looks a r o u n d with anxious g'lancing or searching movements in an inquisitive rammer, u s u a l l y

t o w a r d s the e o n t r a l a t e r a l side. The pupils dilate slowly a n d there ix retra~.tion of the n i c t i t a t i n g m e m b r a n e s with o p e n i n g of the eyes. P r i c k i n g an(1 directional mowqnents of the ears are fre(tuently seen. I)urin~ the stimulation the animal still responds at)l)r()priately to various e n v i r o m n e n t a l stimuli, such as noise, light, mowm]ents within their field of vision, a n d to p i n c h i n g of the skin. However, a l t h o u g h u n d o u b t e d l y (.ons(,ious, lhe reactions to external stimuli are usually somew h a t decreased, the a n i m a l ' s attenlion appears to be a t t r a c t e d a n d intensely fixed on " s o m e t h i n / " which it seems to experiem.e. W h e n a p r o p e r cortical stimulus was applied d u r i n g drowsiness or natm'al or d r u g i n d u c e d light sleep the animal soon, wilhin a few seconds, ai)peared awake amt vi~'ilant aml might ~,o'et llpon its feet. Locali?atio~. The ('ortical sites yielding the behavior attention response are shown in figure 2. E f f e c t i v e lo(d were t'ouml in the following' regions: (it in the medial frontal cortex, the vin~'ulate and hil)l)o(,aml)al ffyri. t'arti(.ularly strong' responses w~'re ol)taim,d from the a n t e r i o r eingulate ~'ortex. N()IIIp points were also locate(1 just lateral to the rhinal fissure, i.e., within the e x t r a r h i n a l (~<)rtex of the t e m p o r a l h)he; (it) in the depth and on the hanks of the presylvian sulcus a n d in the l)roreate ~'yrus on the lateral surfa(,e of the frontal lobe; (iii) in a larg~, zone of the temporo-occipital cortex. W i t h i n lhis z()lle, the 1)est effects were obtailwd from tho h)wer l)ortions of the 1)c)sierior SUl)rasylvian a n d e('tosylvian gyri. A n t e r i o r 1o this r('7'iml, responsive sites, althou~'h with ~ hi~'her threshoht, were scattered in the post~;,,'i()r and a n t e r i o r sylvian and in the antel'i<)r amt middle eetosylvian gyri. Caudally, a f<.;v points were f o u n d on the posterior (.r~*si of the lateral eonv<)luti(m; (iv) a few p<)silive sil(*s, am
577

BEHAVIOR "ATTENTION ' ' AND FEAR (B)

The fear response.

tion response

()n increasing the stimulus intensity the attention response, when induced from eertain cortical sites, developed into a reaction of fear. The searching and glancing movements became more r a p i d ; the animal seemed frightened, would cringe and withdraw a little as if in preparation for flight from sotne unknown threat. The pupils dilated widely. Finally the restless cat would r u n away (the flight response). There were marked signs of fear for half a minute or nlore after the interruption of stinmlation. The fear patteru was similar to that obtained on amygdaloid and brain stein stimulation but was usually

is t h e s a m e as t h a t p r e v i o u s l y

obtained on cortical stimulation in (tats (Kaada 1951; Kaada, Jansen and Andersen 1!)52, 1953; Jansen, Andersen and Kaada 1955-1956; Sano 1958) and monkeys (Segnndo, A r a n a and French 1955). In our opinion at least three components of the con,plex behavior pattern should be distinguished : (i) an initial phase of arrest of all ongoing movements; (ii) increased alertness or arousal; and (iii) movenlents of an ori~nti,..I character, ahnost inw~riably towards the eontralateral side. The terms " a r r e s t rea~tion" (Kaada 1951) and " a r o u s a l " (Segundc., A r a n a and French 1955) only reflect certain

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Fig. 2

Medial (A) and lateral (B) aspects of the cat's hemisphere imlie:lting points (open squares) front which behavior "attention" responses were induced. Dots, no such response. In A 104 electrode positions previously published fronl our laboratory (.lnnsen, Andersen :lnd Kanda 1955-1956) lmve been included; rh ~ rhinnl fissure. less marked and did not always terminate in flight Localization. The eortieal evoked fear response was less frequently obtained than the attention response. I t was particularly vh,ar on stinmlating the cingulate cortex and the lower portions of the posterior sylvian. e~t(>sylvian and suprasylvian gyri. F r o m the other cortical sites yielding the attention response some restlessness and quick and anxious glaneing was frequently evoked but no distinet manifestations of fear, even on maximum strent~th of the stinmlating cnrront. DISCUSSION

A. The behavior " a t t e n t i o n " rcspo~sc. Relation to previous behavior studies with chronically implanted electrodes. The atten-

features of tile eomplex reaction pattern. The behavior arousal which van be elieited from the midbrain reticular fornlation is usually not assoeiated with contralateral movements; the searching is performed in any direction in quite an unpredictabh~ manner. The additional element of orienlation, or directed attention, follows stimulation of teleneephalic (cortical and amygdaloid) and dieneephalic areas (the lhalamie intralaminar, dorsomedial and anterior nuclei). (el. Ursin and K a a d a 1960 a, b). In our experience, behavior arousal ~'an be induced from the meseneephalic rolieular formation at considerably lower stimulus intensities than from the cerebral eortox. Tho amyo'dala and medial thalamus take an interme
578

C H R I S T I A N F A N G E L and B I R G E R R. K A A D A

diffuse electrocortieographic activation elicited from the same structures (Kaada and Johannessen 1960). Retation to the " o r i e n t i n g r e f l e x " . The behavior attention response is similar to and probably identical with the " o r i e n t i n g r e f l e x " of the intact animal first described by Pavlov i. 1910 (see P a r l o r 1928), and by him also variously termed the " i n v e s t i g a t o r y r e f l e x " and " f o c u s i n g reflex". This constitutes a (.mnplex, f u n d a m e n t a l behavior pattern in reaction to any sudden change in the environment and is characterized by an orientatioi~ towards the external stimulus. The investi~zatory or searching behavior is preceded by a phase which by P a r l e y was termed " w h a t is-that" (Russian, shto takoe) reflex. I f the stinmlus is sufficiently strong, the orienting reflex may be associated with marked fear (Robinson and Gantt 1947, p. 233). The orienting reflex is a strong unconditioned reaction: it is present in a wide range of species; it is an inborn and unlearned reaction which is also exhibited by decorti(,ated animals (Robinson and Gantt li)47). It tends to be gradually extino'uished with repetition of a given stimulus, a i)henomenon which does not occur in a decorticated animal. This extinction has been considered to be an instance of cortical inhibition (Robinson and (/antt 1947, I>. 233). ltowever, the present study, and those of the other authors menti
activation can be induced by stimulation (fig. 3 A-B) (Kaada and Johannessen 1960). An a p p a r e n t exception is the separate parietal zone in the lateral and middle suprasylvian gyri. F r o m this region definite generalized E E G activation could sometimes be induced, but no convincing behavior attention, except for a few times when some weak responses were obtained, tIowever, this parietal fiehl was also the weakest of all the areas yielding E E G desynchronization. A similar coincidence has heen found for the cortically evoked behavior (~egundo, A r a n a and French 1955) and E E ( I arousal in the monkey (Se~z'undo, Naqm,t and Buser 1955) (fig. 4 A-B), as well as for the same effects induced from the amy~'dala in cats (Kaada and Ursin 1957; l'rsin aml Kaada 1960a). Generalized E E G activation has also heen elicited from the orbito-insulo-temporal polar cortex in the eat (Kaada 1951 ; Kaada and Johannessen 196(1) and monkey (Segundo, Na(tuet and Buser 1955). This re~'i(>n (lhe orbital gyrus) was not stimulated in the present study. However, comparahlc behavior responses have previously been i)ro(tuced from this field in the eat (Kaada 1951) as well as in the monkey (Se~un(to. Arana and Prem.h 1955). Relation to areas with aJ~ inhibitor!! actioJ~ on mo~,cments. A prominent feature of the behavior attention response is the inhibition of ongoing a(,tivity and movements at the onset of stimulation, " t h e arrest reaction". In the cat, Tower (1936) and K a a d a (1!)51) have mapped the cortical areas which, on excitation, produce a quieting effecl or a prompt and complete arrest of spontaneous movements under light ether (Tower) and barbiturate-chlorah)se anesthesia (Kaada]. These areas (fig. 3 C-D) ch>sely coinride with those yielding behavior attention (fig. 2) and E E G activation (fig. :~ A - B ' ) . This applies to the medial surface as well as to the lateral frontal and temporo-oecipital fields. In the map presented by Kaada (1951, fig. 22), the latter fieht is somewhat less extensive and divided into two fields, a temporal and an occipital. This pr(d)ably is duo to the deeper anesthesia used in these experiments. IVnder favourable oonditi(>ns,

579

BEHAVIOR ' ' ATTENTION ' ' AND FEAR

the responsive area had the same extent as found by Tower. I n addition, K a a d a found that arrest of movements was also readily produced f r o m p a r t of the p y r i f o r m cortex and the orbital g y r u s (fig. 3, stippled), and area not explored by Tower, and p r o b a b l y the homologue of the orbito-insulo-temporal polar re~ion of primates ( K a a d a 1!)51, pp. 78-8(i).

Both investigators also obtained some but h, ss constant quieting effects from the parietal cortex (the lateral and middle suprasylvian g y r i ) , thus including most of the t e r r i t o r y between the somesthetic and visual fichts. The inhibitory action was not interf(,r(~d with by sectioning the p y r a m i d s at a medullary level (Tower 1!)36 ; K a a d a 1951 ). ." .'t.':"

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Fig. 3 C a t ' s br:dn. A-B. Cortical diagr'nns indicating points (filled circles) from which generalized clectrocortical desynchronization could be induced by elec trical stimulation. Dots, no such effect ( K a a d a and J o h a n n e s s e n 1(.)60). C-I). Horizontally shaded: extraI)yramidal cortical areas for inhibition of spontaneous somatolnotor movements, as determined by Tower (1936). Similar results obtained by K a a d a (1951). Dotted zones: additional areas for inhibition of movements as determined by K a a d a (not explored by Tower) (cf. t e x t ) . Diagonally shaded: frontal, parietal and occipital contraversive fields ('ffter Tower 1936). E. AroM division on the medial surface, ~,ccording to Rose and Woolsey (1948). Cg z cingular area; cr = crucinte sulcus; I1 _-- infr.dimbic "lrea; La -a n t e r i o r limbic region; Of __~- o r b i t o - f r o n t a l region; P r a g _~ precentral agranub, r area; Ps ~ p o s t s u b i c u l a r a r e a ; rh _~ rhinal f i s s u r e ; Rs ~ retrospl,.,nial arc:,; spl __-- splenial sulcus. - - F. Localization of the f i r s t and second visual, auditory a n d somatic sensory fields as defined by the evoked potential method. Black area represents the m o t o r field as determined by electrical stimulation ( r e d r a w n f r o m Rose and Woolsey 1949).

580

C H R I S T I A N F A N G E L a n d B I R G E R R. K A A D A

i t seems nmst likely that the inhibitory influence on movements exerted b y these fields merely represents a f r a g m e n t of the total behavior attention response as seen in the non-anesthetized animal. I t should be emphasized that the action of all these cortical fields was p r i m a r i l y on movements, randora or rhythmic. They were also effeetive against the j e r k y movements induced by sensory stimuli in ehloralosed aninmls ( K a a d a 1951). They were quite ineffective (with the exception of the pre- and subeallosal p a r t of 1he anterior cingulate area and p a r t of the orbital gyrus) against tonic contractions in 1he musculature ( K a a d a 1951). On the eonlrary, Tower (1936, p. 419) described the action of the inhibitory fields for movements, at a maxinmm, as one involving " . . . strong ~onie innervation, either as tonic extension or as tonie innervation of all the museulature producing semi-flexion", suggesting " . . . a reversion of control to the tone producing mechanism when nmvement is a r r e s t e d " . The attitude of the animal was deseribed as " a ,,haraeteristic a p p e a r a n c e of fixation at atlenl i o n " . The eontralateral searching movemeats, absent in the anesthetized eats, a p p e a r ~o be a eharaeteristie of the fully conscious animal. The generalized inhibition of movements also includes breathing whieh m a y become slow (with full or decreased excursions) or cease. D u r i n g lighter anesthesia, however, it nmy also become shallow and r a p i d (Tower 1936 ; K a a d a 1951, 1959). Also, in the mo~key the eortieal sites yielding the behavior attention response (fig. 4 A-B, filled squares) (Segundo, A r a n a and F r e n c h 1955) and generalized E E G desyn~dtronization (Sloan and J a s p e r 1950b; K a a d a 1951; Segundo, Naquet and Buser 1955) all a p p e a r to be located within the areas exerting an inhibitory action on movemcnts (ef. fig. 4 A-B and C-D). This applies to the inhibitory fields of the medial surfaee ( Bailey ct al. 1944 ; Smith 1945 ; K a a d a 1951 ). ~he intermediate lateral frontal field (mainly 1he lateral portimts of areas 8 and 9) (Mettler 1942, 1948; Hines 1943; K a a d a 1951), the posterior orbital, anterior insular and temporal polar fields, the superior

temporal g y r u s ( K a a d a 1951) and the paraoccipital region (area 19) (Dusser de Barenne, Garol and ~{eCulloeh 1941). The two latter fields arc p r o b a b l y included in " t h e junctional zones of the three posterior lobes" f r o m which Itines (1943) elicited inhibition of movements. The relation of the eortieal zones for i n h i b i t i o n of m o v e m e n t s to the so-called " . ~ p p r e g x o r " ar~'as 8s, 4s, 2s, 19s a n d 24s ( D u s s e r de B a r e n n e a n d MeCulloeh 1941; D u s s e r de B a r e m m , Garol a n d McCulloeh 1941; Garol 1942a, b; Bailey #t al. 1944; MeCulloeh 1944) h a s been discussed ill detail elsewhere ( K n a d a 1951, p. 93 a n d p. 139: 1952, 1959). I t s u f f i c e s here to m e n t i o n th'~t one of the v a r i o u s m o t o r i n h i b i t o r y e f f e c t s r e p o r t e d by these a u t h o r s to be a clmraeteristie of the ' ~ s u p p r e s s o r " strips, the r e l a x a t i o n of m u s c u l a r c o n t r a c t i o n s a n d the tess;ilion Of 8polltl/lleOi18 Inovelllelltst vcas gait] to fll)l)eaF a n d d i s a p p e a r p r o m p t l y on s t i m u l a t i o n (McCulloeh 1911; Garol a n d Buoy 1944). T h i s intmedi~,te reSlmnse s t a n d s in s h a r p e o n t r a s t to the ~ ' s u p p r e s s i o n of electrical a c t i v i t y " a n d the " s u p p r e s s i o n of the m o t o r reslmnse to s t i m u l a t i o n of urea 4 " , both of which a p p e a r e d a f t e r a r e m a r k a b l e long l a t e n c y of sever-i1 m i n u t e s . S]oan a n d J a s p e r (1950n) have b r o u g h t f o r w a r d convincing evidence t h a t these h m g l a t e n c y eleetrieal "rod m o t o r responses, which were originqlly elicited only front the speeifie cortieM " s u p p r e s s o r " strips, are m o s t p r o b a b l y identical to the ~ ' s p r e a d i n g depression '~ of LeSo (1!)44), a phen o m e n o n which is non-specific in t h e sense tlmt it c~n be elicited f r o m a h n o s t a n y portion of thv cerebral cortex.

Thus, although considerable doubt has been east ut>on the existenee of specific " s u p p r e s s o r " areas, this doubt o n l y e o n e e r n s those studies in which they have been deliminated by the lon~'-lateney responses. The immediate inhibition of movements front the areas in ¢tuestion have, on the whole, been confirmed in subsequent studies (el. K a a d a 1!151 ) ) With some minor exceptions the " s u p p r e s s o r " strips 8s, 2s, 19s and 24s are all found within the cortical areas for inhibition of movements, as outlined abow~ for the eat and monkey. However, when tested u n d e r lighter anesthesia each of these inhibitory zones has a somewhat wider extent than the narrow " s u p p r e s s o r " strips, b~urther, in addition to the intermediate frontal (8s), parietal (2s), ot.~-ipital (19s) and eingulate (24s) fields, an orbito-insulo-temporal polar and a total)oral

BEHAVIOR ' ' ATTENTION

zone should be included in the cortical fields for inhibition of movements. I n conclusion, the functional significance of the inhibition of spontaneous movements as induced f r o m eortieal fields, including the much discussed " s u p p r e s s o r " areas, is probably related to the attention response, as also previously suggested by one of us ( K a a d a 1!}51, p. 146; 1952, 1!)59).

' ' AND FEAR

5~1

Rotation to the cortical association areas. The cortical sites yielding behavior attention (fig. 2) and E E G desynehronization (fig. 3A-B) on excitation are ahnost entirely loeated, within the association areas, i.e. in the fields between the various p r i m a r y sensory projection areas and the frontal motor area (fig. 3P). ttowever, a few points were also found within the p r i m a r y acoustic and visual

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Fig. 4 M o n k c y ' s brain. A-B. Composite cortical d i a g r a m s i n d i e a t i n g p o i n t s f r o m which eleetroeortieal d e s y n c h r o n i z a t i o n eouhl be indue~,d with ( d o t t e d circles) or w i t h o u t (filled circles) localized cortical a f t e r d i s e h a r g e . Open circles indicate cortical a r e a s t e s t e d w i t h o u t i n d u c i n g d e s y n c h r o n i z a t i o n ( r e d r a w n f r o m S e g u n d o , N a q u e t a n d B u s e r 1955). Filled s q u a r e s z behavior " a r o u s a l " with i n t e n s i t i e s u n d e r 12 V. tIalf-filled s q u a r e s behavior " a r o u s a l " with i n t e n s i t i e s over 20 V. Open s q u a r e s = no b e h a v i o r " a r o u s a l " ( r e d r a w n f r o m S e g u n d o , A r a n a a n d F r e n c h 1955). C-D. Composite d i a g r a m s i n d i c a t i n g a r e a s ( d o t t e d a n d horizontally s h a d e d ) y i e l d i n g p r o m p t i n h i b i t i o n of s p o n t a n e o u s m o v e m e n t s . H o r i z o n t a l l y slmded = the " s u p p r e s s o r " a r e a s 8s, 4s, 2s, 19s a n d 24s ( a f t e r D u s s e r de B a r e n n e , Garol a n d MeCulloeh 1941; B a i l e y et at. 1944). D o t t e d zmws _-2 a d d i t i o n a l a r e a s c a u s i n g i n h i b i t i o n of m o v e m e n t s , in t h e f r o n t a l a n d telnporal lobes a n d a n t e r i o r i n s u l a ( a f t e r K ' m d a 1951). T h e a r e a s d e t e r m i n e d b y K a a d a also include a r e a s 24s a n d 8s. E - F . T h e m o n k e y ' s a s s o c i a t i o n cortex as d e t e r m i n e d b y eytoarehiteetonies. I t consists of the e u l a m i n a t e cortex ( s t i p p l e d ) , t h e l i m i t r o p h i e zones ( h a t c h e d ) , nnd possibly t h e a n t e r i o r e i n g u l a t e (limbie) region ( c r o s s e d ) . The u m n a r k e d a r e a s are p r i m a r y p r o j e c t i o n a r e a s ( a g r a n u l a r cortex a n d konioeortex) a n d alloeortex ( A ) . T h e d e s i g n a t i o n s of cortieal a r e a s are those of von B o n i n a n d Bailey (letters) a n d B r o d m a n n ( f i g u r e s in p a r e n t h e s e s ) . ( S l i g h t l y nlodified f r o m Chow a n d H u t t 1953.)

589

CHRISTIAN FANGEIJ and BIRGER R. KAADA

projeetion fields (fig. 2B), and it is possible that in these instances the attention response might be secondary to a sensory experience. Therefore, as the behavior attention evoked from these points may have a different funetional signifieam:e, they should possibly be exeluded. This also applies to the few points located within the first and second motor areas from which the behavior attention was accompanied by innnediate muscular contractions Also, no generalized E E G desynehronization was obtained, in the lightly anesthetized animals, from the p r i m a r y sensory areas, ex~el)t in a few instances with very strong stimulation (Kaada and ,lohannessen 1960). Finally, it requires far' more intense stimuli to arollse atl animal froul natural sleep when stimulating a l)rimary sensory field than a non-sensory area (Segundo, A r a n a and l'h'enuh 1955). A more exact i)areellation of the cortical attention zones in relation to the various ,ytoarehiteetonic Fields within the association areas can at present only be tentative. However, fronl the data obtained, both in the cat and monkey, it is perhaps permissible to conclu(le that in the oeeipital, temporal and parietal lobes the attention response in related to the l)arasensory fields of the visual, acoustic and somesthetie areas. Similarly, the :-ittention response induced front the orbitoinsulo-temporal polar eortex is possibly associated with the parasensory olfaetory, gustatory and wtg'al fields of these regions. The ~.ingulate and lateral frontal respot,sive fields are developed independently of any known sensory projection areas. All these parasensory fields appear r(mghly to eoineide with the so-called " l i m i t r o p h i e " cortex (Benin and Baily 1947; Bailey 1948; Bailey and Benin 1951) which represents a transitional or fringe zone between the eulaminate type of the remainder of the association cortex and the p r i m a r y sensory an(t the preeentral motor fields (horizontally shaded in fig. 4 E - F ) . One eharaeteristie of these transitional zones is the unusually large pyramidal <,ells in the deeper part of the third layer ( B e n i n and Bailey 1947; Bailey 1948 : Bailey and B e n i n 1951). To these zones

of limitrophie cortex ( d y s g r a n u l a r cortex of the intermediate frontal region; parakoniocortex of the occipital, posteentral and supratemporal reg'ion; juxtalloeortex of the posterior orbital, anterior insular, and anterior and inferior temporal regions) the anterior cingulate area should possibly be ineluded (Chow and l I u t t 1!)53). This attribution of the attention zones to the limitrophic fringe zones is only tentative and requir,,s verifi~,ation in future experimentation. Relalio~ to a~tto,omic arcas. The arousal front slee 1) to wakefuhwss and the attention reaction are associated with a mmlber of atmmomic effeets Slll*h its pupilha'y dilatation, <,hanges in respiratory rhythm, in hearI rate, blood i)ressure, etc. Su(,h responses have been obtained front most of the ('ortieaI ar,,as concerned by a number of earlier investiR'ators. In fact, the cortical auton()mi~, rel)resentation corresponds t() a great extent t,) the corticM attention areas. This in well (lommwnted for the medial asl)eet of lh(' hemisphere, the orbito-insulo-temp(.'al polar region, and tit(, lateral intermediate frontal a r e a in both the eat and the monkey (for summary, see K a a d a 1951, 1960; I)ell 1952). With regard to the temporo-occil)ital and parietal fields, Sane (1!)58) has recorded pupillary dilatation and salivation on stimulating' the lower ends of the posterior sylvian, e,tosylvian and suprasylvian ~'yri in the ~,at. In the monkey, respiratory inhibition tnLq been obtained front the superior temporal ,.,'yrus (Kaada 1951). Like the inhibition of movements, some of the variotls autonomic reactions observed tamer anesthesia probably represent frao'ments of the attention respollse, and are, under normal eondititms, integrated in this total behavior pattern. In this way, tit(, fum'tional signifieaneo of some of the .ortieal autonomic responses may possibly be explained. R d a t i o n to conl'raversfrc fields. Sim,e the searchin~ movements of the cortically indueed attention response are ahnost invariably direeted towards the eontralateral side, it may be of significance that the elassieal eorti(,al eontraversive fiehls are located in close

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~ ~A T T E N T I O N

association with the areas yielding the attention response, although it cannot be said that the two entirely coincide. I n the monkey, eontraversive fields are found in the intermediate frontal and in the parasensory visual, acoustic and somesthetie areas (Hines 1943). Also, in the same species contraversive movements have been described on stimulating the cingulate and orbito-insuh)-temporal polar region (Kaada 1951). I n the eat, the lateral frontal, parietal and occipital contraversive fields, as mapped by Tower (1936) in lightly etherized animals, are shown in figure 3 D. In addition, contraversive movements have been obtained from the cingulate (Hess 1948; Kaada 1951) and hippocamI)al gyri (Kaada 1 9 5 1 ). Certainly, typical attention responses with contralateral orientation were also obtained from areas outside the well-known contraversive fields. F u r t h e r , the searching movements of the attention response differ somewhat iu character from the tonic t u r n i n g of the head and t r u n k produced by electrical stimulation of the classical lateral contraversive fields, or seen when epileptic discharges involve the same regions (l)enfield and Kristiansen 1951; Penfield and Jasper 1.(t54). A different mode of activation may aeeouut for this difference in character. W h e n im.reasing the stinmlus strength it was sometimes seen, in the present study, that the contralateral searching was replaced by a strong tonie contraversion. It appears quite possible that this cortical mechanism for eontraversion under physiological conditions is in some way integrated in the attention response, and m a y be lhe one responsible for the animals' orientation to the eontralateral side. Fl~ctio~al sig,ificance. The (,lose resemblance of the stereotyped attention response elicited from the cerebral cortex, amygdala and medial thalamus to the orienting reflex of P a r l e y makes it likely that they have a similar functional meaning in normal life. The orienting reflex, also present in de(.orticated animals (Robinson and Gantt 1947 ), is a vital reflex, serving to detect any external threat and to guide the animal in its environment. It appears as if the same

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basic orienting behavior pattern is organized at a higher cortical level as well. The cortical zones concerned a p p a r e n t l y have access to the same subcortical mechanisms which mediate the externally induced reflex. Further, through this cortico-subcortical mechanism the cerebral cortex possibly coutributes to the initiation and maintenance of wakefulness and alertness. How the cortical attention response ~,omes into play in normal life can only be a matter of speculation. The localization of the effective areas to the fringe zones of the ass()elation cortex adjacent to the p r i m a r y receptive fields might suggest an activation of the attention mechanism through an inlet'ration of perception and mental activity. The frontal lobe and the eingulate eortt~x both have their own attention zones, (mrela~ed to any known sensory system, llowever, although these diverse cortical zones a p p a r e u t l y have some common functions relate(I to alertness an(t attention, it appears mdikely, as also emphasized by French. ilernfin(tez-l)edn and Livingston (1955) and Kaada (1960). that all influences mediated hy them are identical, or that these are the only fum.tious they subserve. Alertness and directed attention associated with activation of the various cortical areas is probably related to a great variety of fuuctional activities such as sensory experience, emotions and higher mental proceses, llence it is not surprising that the same behavior pattern, associated with ele(~trocorticographic arousal, can he induced fr(>m fairly wi(lespread but distinct (q)rtieal and subeortieal areas. The subeortical substrate for the orienting reflex and for the teleneephalic induced atteution response is not known. A commou projection field for corticofugal impulses from the areas in (tuestion appears to be the hrain stem reticular formation, as demonstrated by electrophysiological methods (Fren(,h, llernfindez-Pedn and Livingstou 1955). A(,eor(1ing to Tower (1936), the inhibition of movements from the cortex probably takes place at a thalami<, level. The abolition (,[' the attention response, induced from the medial frontal cortex in the cat, by lesions of part

584

CHRISTIAN FANGEL and BIRGER R. KAADA

of the intralaminar thalamie nuclei (Jansen, Andersen and Kaada 1955-1956) is consistent with Tower's assumption. (For further dis~,ussion of this problem, ef. Ursin and Kaada 1960b.)

t;. The fear response. Fear as a result of cerebral cortical stimulation has previously been obtaiued in the (.at from the cingulate and hippocampal gyri (Kaada, Jansen mid Andersen 1953), and from the lower end of the posterior suprasylvian gyrus (Sane 1q58). In the monkey, Se~zundo, A r a n a and French (1!)55) observed fear and escape reaction on exeitation of their cortical ' ' a r o u s a l " areas outlined above. However, they do not specifically state whether there were any regional differences. I n the animal experiments, fear (flight), whether evoked from cortical or subcortical sites, is always preceded by behavior arousal or attention. At subeortieal lew~ls fear has 1)een produced by stimulation of the amygdala (for references el. Ursin and Kaada 1960a; Ursin lq60), the medial thalamus, the hypothalanms and the meseneephalie reticular formation (Hess 1954; Delgado et al. 1954, 1!)56; Segundo, A r a n a and French 1955; YamaR'uehi 1956, ciL Sane 1958; K a a d a and Bruland 1960). All these zones appear to be located within the meseneephalie, dieneephalic aud teleneephalic arousal or attention areas. The results from our laboratory indicate that the fear response - - like the induced b(,havior attention and E E O activation ~-has its lowest stimulus threshold in tile mesen(~ephah)n and h y p o t h a l a m u s ; next comes the mnyRxtala, whereas still higher stimulus intensities are required to elicit the effects (m ('ortical stimulation. Anesthesia abolishes lhe response in the reverse order, the mesen~,ephalic evoked response being the most persisteut one. The present study also permits a (,omparison between the various cortical re,.,'ions. ,qome (]eg'ree of anxiety appears to be part of several, althou~'h hy far not all. attenti(m responses, as judged from the induced restle~sm,ss and the anxious and quick ,A'lan(,inR' movements, particularly on relative strong stimulati(m. IIowever, definite man-

ifestations of fear, resulting in flight, were only induced from a few points iLL the lower ends of the posterior sylvian, eetosylvian and snprasylvian gyri and from some electrodes placed in the eingulate eortex. Thes,, were also the cortical regions yielding the best an(l most consistent behavior attention and E E G activation responses in the eat (Kaa(la and Johannessen 1960) and monkey (Segundo, Ararat and Freneh 1955). Relation to fear ill cpilcptic seizures. Fear and anxiety as manifestations of epileptic anra have commonly been desm'ihed as temporal in orio'in ( I ' e n f M d and Kristiansen 1!151 ; Macrae 1954; P e n f M d and Jasper 1954 ; Gastaut, Morin and 13esevre 1955; (libbs 1!)56; Well 1956; Williams 1956; lling'ley 1958). The epileptogenic (liseharg,.s corm'lated with the feelings of fear are usually found in the anterior or mid-temporal region. F6ster, Castells and E t e h e v e r r y (1954) reported that epileptic sleep terrors w,re asso(,tared with a cortical ]~]E(I t'oeus in the parieto-t en,poro-oecipital area. It is difficult, however, from such observations to determine the exact h)calizatiml of the nervons substrate within the temporal lobe responsible for the paroxysms of fear. Epilet~togenic discharges from a eorli(.al focus may spread to tile amyg'dala and ,ic~' rr~sa. More importam.e ean probably be atta<'he(1 to slimulation experiments. The animal studies demonstrate that lemporal ('ortieal as w,I1 as amygdaloid stimulation may elicit f(,ar rea,tioHs. These results are (,onsistent with similar observations by stimnlation in m a . (for review, see l:rsin 1960). IIeath. Monroe and Mickle (1955) stimulated the tmlyR'(lala in a sehizophrenie patient who dovehqLed intense fear with an impulse to run. (lhapmau (1956) produced a sensation of fear , r fright in 4 of 6 epileptics on stinmlalion of ~he amygdaloid region throuo'h implaW, ed electrodes. I n the experience of Jasper .n(l Rasmussen (1956), feelincs of fear wer,' evol(ed in only 2 of 46 epileptic patients (m amy~'dala stimulation (luring' opm'ati(m, l'enfield and Jasper (1!)54) and Penfi(dd (1956) produced feelings of fear, sadness, friR'ht and terror in epilepties on stimulalinR" tl)e cortex

BEHAVIOR

' ' ATTENTION

of the anterior and inferior surface of the temporal lobe. All these studies may be taken to indicate that reactions of fear may be initiated from temporal cortical as well as amygdaloid neurons. TILe observations iil hmnans are of great imt)ortanee in so far as they clearly demonstrate that the induced reactions of anxiety and fear are not due to pain or to any other somatic sensation nor are they secondary to thought processes. The evoked fear has no otLject, is um,.eountable to the patient and, according to Heath et al. (1955), it is integrated in the normal thinking of the patient. It is also (if interest that the centrally induced fear in eats has been shown to possess lhe functional prol)ertics of normally elicited fear (l)elgado, Roberts and Miller 1954). Thus, fear induced by stimulation of the amygdala, lhalamus and mesencephalon could be used t~) motivate l e a r n i n g , to establish a eonditi(med response, and to serve as a punishment to eslablish an al)proach-avoidanee conflict. Whereas stimulation of the amygdala, in addition to the fear response, also yields a tyl)ical anger or rage reaction, such an effect was never cncoulltered ()n cerebral cortical stimulation. Gastaut ¢t al. (1952) state that the anger response obtained from the amygdala ill cats is a f u r t h e r development of the fear reaction: stimulation of the same point wilh a gradual increase of the intensity first resulted in the attention response, then fear, and t'inally rage. ()n the other hand, lrrsin and Kaada (li)60a) interpreted the fear and anger responses, both preceded by behavior atiention, as two distinct and different types (Lf emotional pattern which were r('lated to two separate areas within the amygdaloid mlclear complex. The failure to produce any signs of anger on cortical stimulation lends s u p p o r t to the assumption that anger is a behavior pattern distinct from fear, as also maintained by most animal psychologists (el. Mor~'an and Stellar 1950). Also, rage reac!ions have. to the authors knowledge, never been reported on cortical stimulation in man. whereas such effects have been produced on amygdala stinmlation (Heath et al. 1955).

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SUMMARY

1. The cerebral cortical areas have been determined from which a behavior " a t t e n t i o n " response can be induced by stimulation in the unanesthetized cat. Three eonq)onents may be distinguished in this behavior p a t t e r n : (i) arrest of all ongoing si)ontaneous mow,merits; (ii) increased alertness; and (iii) orienting movements towards the contralatcral side (fig. 1). The response is probably identical with the " o r i e n t i n g r e f l e x " described by Pavlov. 2. The responsive areas include: (i) the cortex of the medial frontal surface, th,. eingulate and hippocampal g y r i ; (ii) the intermediate lateral frontal cortex; (iii) a large temporo-occipital field; (iv) the orbito-insular-temporal polar region ; and ( v ) a w e a k e r parietal field. These cortical zones eorresl)oml t(L those from which a generalized electrocortical activation have been elieited i , the cat and monkey (fig. 3 A-B and 4 A-B). Cytoarehitectonieally, they appear to he related to the " l i m i t r o p i e " type of association cortex (fig. 4 E - F ) . 3. The positive areas coincide with those previously known to produce inhibition of spontaneous movements, various autoll()nlie effects and contraversion (fig. :l C-I) and 4 (!D). These responses, obtained ml(ler aLLesthesia, are interpreted as parts of the ('omplex behavior " a t t e n t i m F ' pattern evoked in the unanesthetized animal. 4. Fear resulted from stinmlation ()t' the eingulate and tenLporo-oceipital em'tex. Its relation lo fear in el)ilelLtie seizures is discussed. m;'SUM~:: 1. Les aires corticales du cerveau out 6t6 d6termin6es o6 par stimulation 61ectriquc sur le chat non-anesth6si6 un comportement attentif pent 6tre induit. Trois composantes peuvent (Xtre distingu6es dans cc comportement: i) arr~t de tous los mouvements spontan6s en progrbs au moment du d6but de la stimulation, ii) vigilance accrue, et iii) mouvement d'orientation Yers le c5t6 contralat6ral (fig'. 1). Cette r6ponse est probablement i(lentiqne

586

C H R I S T I A N F A N G E L a n d B I R G E R R. K A A I ) A

avee le <> d6crit p a r Parlor. 2. Les aires h p a r t i r desquelles eette r6action peut ~tre induite sont les suivantes: i) le cortex de la face m6diale du lobe fronlal, la circonvolution limbique et la circonvolution de l ' h i p p o e a m p e ; iX) le cortex frontal lat4ral interm6diaire; iii) une aire 6tendue lemporo-oeeipitale; iv) la r6gion orbitah, insulaire et ]e p61e temporal et, finalement, v) mm aire pari6tale moths effieaee que les autres. Ces aires eortieales correspondent (,ell(+s il p a r t i r desquelles mm aetivation g6n6ralis6e de l'aetivit6 eortieale pent ~tre induite chez le chat et chez le singe (fig. 3 A-B et 4 A-B). Du I)oint de vue eytoarehiteetural ees aires semblent ~tre apparent6es au type <~limitrope >>du cortex assoeiatif (fig. 4 - E - F ) . 3. Les aires effieaees coincident avee ee]les (.ommes pour ~tre eapable de produire m~e inhibition des mouvements spontan6s, d ' i n duire des effets v6g6tatifs vari6s et des d6vialions contraversifs (fig. 3 D-G et 4 C-D) C*es r6ponses obtenues sous anesth6sie sont interpr6t6es eomme faisant p a r t d ' u n eomportemerit a t t e n t i f c<)mplexe produit chez le chat non-anesth6si6. 4. lhl eomportement de p e u r est induit p a r des stimulations appliqu6es au cortex limbique et temporo-oeeipital. La relation du comportenmnt anxieux observ6 darts les crises 6pileptiques avee eette r6ponse h la slimulation 61ectrique est diseut6e. Z US A M M E N F A S S U N G

1. Es wurde bestimmt, yon welehen H i r n r i n d e n r e g i o n e n eine verhaltensmiissige "Aufmerksamkeits"-Reaktion hervorgerufen werden k m m dureh Stimulation in nicht-narkotisierten Katzen. Drei K o m p o n e n t e n kSnhen in dieser Verhaltens-Reaktion mltersehieden werden : (i) Hemmung aller s t a t t f i n d e n d e n spontanen B e w g u n g e n ; (iX) gesteigerte W a e h s a m k e i t ; (iii) orientierende Bewegungen zur Gegenseite (Abb. 1). Die g e a k t i o n ist vermutlieh identiseh mit dem Pawlowsehen " ( ) r i e n t i e r u n g s - R e f l e x " . 2. Zu diesen Regionen geh5ren: (i) die mediale Stirnhirnrinde, die gyri einguli lind h i p p o e a m p i ; (iX) die intermediiire laterale g t i r n h i r n r i n d e ; (iii) ein grosses temporo-

oceipitales F e l d ; (iv) die Region bestehend aus der orbitalen und Inselrinde und iv) ein sehw~ieheres parietales Feld. Diese Rindenfelder entsprechen denen wm welchen generalisierte elekrokortikale Aktivation erreicht wurde in der Katze und beim Allen. (Abb. 3 A, B u n d 4 A, B~. Zytoarchitektonisch stehen sie anscheinend in Beziehung zum " / i m i t r o p i s e h e n " T y p (h'r Assoziationsrinde (Abb. 4 E, F ) . 3. Die positiven Gcbiete sind (tie gleiehen wie diejenigen welche sehon friiher dafiir bck a n n t waren, dass sie tlemmu)~g v())l Spontanbewegungen, verschiedene alltollollle Effekte un. (*oncerning the <)rg:,nizntion of the c(.rebral cortex. Tex. Rcp. Biol. Me'd, 1948, 6: 34-56. ]:IAILEY, P. "l.Ild ]~ONIN, (~. VON. 7'hr Isocortex of Man. U r b a n q , ['niv. of Illinois Press, 19,57, 301 pp. BAILEY, P.~ B:ININ, (I. ,,'ON, DAVIS, E. \V., GAROL, H. W., ~ICCULLOCII, W. S., ROSEMAN, E. a n d SILVEIRA, A. Fm,ctioIml organiz:ltion of the medial a s p e c t of the p r i m a t e cortex. J. N<'orophysiol., 1944, 7: 51-56. B1NGLEY, T. M e n t n l s y m p t o m s in t ( m p o r a l lobe epilepsy a n d t e m p o r a l lobe gliomas. Actn psychiat. ( K b h . ) , 1955, 33 (suppl. 1 2 0 ) : 1-151. BONIN, G. VON a n d It~A1LEY, 1). The' Ncocortcx of Macactt Mulatta, U r b a n a . Univ. of Illinois Pres~, 1947, 163 pp. CHAPMAN, W. P. S t u d i e s of the p e r i a m y g d a l o i d qre', in relation to h u m a l t belmvior. Rex. Pttbl. Ass. herr..mont. Dis., 1986, 36: 258-277. CHOW, K . L. a n d HUTT, P. ,I. The " a s s o c i a t i o n cort e x " of Macaca nodatta: A review of recent c o n t r i b u t i o n s to its a n a t o n , y a n d f u n c t i o n s . Brain,

1953, 76: 625-677. ])ELGADO, J. ~[. R., ROBFRTt--;, W. 'W. ;lit(| ~IILLER, N. l~earning m o t i v a t e d by electrie:ll s t i m M a t i o n of the brain. Amr'r. J. Physiol., 1954, 179: 587-59a. DELCADO, .~. M. R., ROSVOLD, lI. ~0~. :HHI LOONEY, E. E v o k i n g conditioned f e a r by electrical stimulation of snbcortieal s t r u c t u r e s in the m<)nkey brain. J. comp. PhysioL Pxychol., 1956. 19: 3 7 3 3 g 0 .

BEIIAVIOR ' ' ATTENTION DELL, I ). Corr61ations e n t r e le syst6me v 6 g 6 t a t i f et h, s y s t 6 m e de la vie de relation. M 6 s e n c @ h a l e , dienc6phale et cortex c6rSbral. J. Physiol. Path. g(:n., 1952, 44: 471-557. DUSSER DE BARENNE, J. G., GAROL, I~I. W. and MC('.ULt~OClt, W. S. F u n c t i o n a l o r g a n i z a t i o n of sensory a n d a d j a c e n t cortex of the m o n k e y . . 1 . Neurophysiol., 1941, 4: 324-330. DUSSER DE BARENNE, J. G. qnd ~fCCULLOCI[, W. S. S u p p r e s s i o n of m o t o r response o b t a i n e d f r o m area 4 by s t i m u l a t i o n of a r e a 4s. J. N e u r o p h y siol., 1941, 4: 311-323. FRENCH, J. D., J{ERN+~.NI)EZ-PE(~N, R. and LIVINGSTON, R . B . P r o j e c t i o n s f r o m cortex to cephalic b r a i n s t e m ( r e t i c u l a r f o r m a t i o n ) in monkey. J. New, tophysiol., 1955, 18: 74-95. ]~'I."STER, B., CASTELLS, C. a n d ETCHEVERU~', M. Epileptic sleep terrors. N e u r o l o g y , 1954, 4: 531-540. GAROI,. H. W. [. The " m o t o r " cortex of the cat. d. Neuropalhol. exp. Neurol., 1942a, l : 139-145. G,XROI,, H. W. I I . T h e f u n c t i o n a l o r g a n i z a t i o n of ~he sensory cortex of the cat. J. Neuropalhol. <.rp. Yearol., 194,2b, 1: 320-329. GAbOn,, It. W. a n d B u o y , P. Supl)ression of m o t o r resi)onse in nmn. Arch. Nc~rol. Psychiat., Chi('ago, 1944, 5 1 : 5 2 8 532. GASTAUT, IT., MORIN, (]. Pt LESEVRE, ~N*. Etude du COml)ortemcnt des 6pileptiques p s y c h e m o t c u r s d a n s l ' i n t c r v a l l e de leurs crises. A n ~ . m:d.-p,~yehol., 1955, 1: 1-27. GASTAUT, H., NAQUE'r, R., ¥IGOUROUX, R. et CORRIOL, .I. P r o v o c a t i o n de c o m p o r t e m e n t s 6motionnels divers p a r s t i m u l a t i o n r h i n e n c 6 p h a l i q u e chez le c h a t avec 61ectrodes h demeure. R('r. neurol., 1952, 86: 319-327. G1BBS, F. A. A b n o r m a l electrical activity in the leinporal r e g i o n s a n d its r e l a t i o n s h i p to ahnorrealities of behavior. ICes. Publ. Ass. ncrv. meat. Dis., 1956, 3 6 : 2 7 8 294. HEATIt, R. (~., 5[ONR'OE, R. R. a n d MICKI,F, W. A. S t i m u l a t i o n of t h e a m y g d a l o i d n u c l e u s in a schizophrenic p a t i e n t . A.mer. J. Psyehiat., 1955, [1l : 862-863. ttEsS, W. R. K o r r e s p o n d i e r e n d e S y m p t o m e a u s Stirnhirn, I n n e r e r K a p s e l u n d v o r d e r e m T h a l a m u s . Ileb,. physiol, pharmacol, acta, 1948, 6: 731-738. It ~:ss, W. R. The 1)i~ neephalon. A u t o n o m i c a~d E.rtraP y r a m i d a l Functions. G r u n e a n d S t r a t t o n , I n c , New York, 1954, 96 pp. H1NFS, ~[. Control of nlovenlcnts by the cerebral cortex in p r i m a t e s . Biol. ICev , 1943, JS: 1-31. JANSEN~ J. ,JR., ANDERSEN, P. a n d }(AAI)A~ ]7~. R. Subcortical m e c h a n i s m s involved in the " s e a r c h i n g " or " a t t e n t i o n " response elicited by prefronttfl cortical s t i m u l a t i o n in u n a n e s t h e t i z e d cats. Y a l e J. Biol. Med., 1955-1956, 28: 331-341. JASPE,¢, H. ]I. a n d RAS~[USSEN, T. S t u d i e s of clinical a n d electrical responses to deep t e m p o r a l stimulation ill a l a n w i t h some c o n s i d e r a t i o n s of func tional a n a t o m y . Res. Publ. Ass. *terv. meat. Dis., 1956, 36: 316-334. I~AADA, ]:~. l~. S o m a t o - m o t o r , a u t o n o m i c a n d elcctroeorticographie responses to electrical s t i m u l a t i o n of " r h i n e n c e p h a l i c " a n d other s t r u r t u r e s in p r i m a t e s , cqt a n d dog. A c t a physiol, scan&, 1951, 2 t (suppl. 83) : 1-285. KAAOA, B. R. The a n a t o m i c a l s u b s t r a t u m of consciousness in the l i g h t of recent n e u r o p h y s i o -

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