Disconnection of the Amygdala from Visual Association Cortex Impairs Visual Reward-Association Learning in Monkeys

Transcription

1 The Journal of Neuroscence, September 1988, 8(9): Dsconnecton of the Amygdala from Vsual Assocaton Cortex mpars Vsual Reward-Assocaton Learnng n Monkeys E. A. Gaffan, Davd Gaffan, and Susan Harrson Department of Psychology, Readng Unversty, Readng RG6 2AL, and Department of Expermental Psychology, Oxford Unversty, Oxford OX1 3UD, England Cynomolgus monkeys (Macaca fascculars) were traned n a task that assessed ther ablty to assocate vsual stmul wth food reward. Acquston of stmulus-reward assocatons was measured under 2 condtons, a 2-stmul acquston condton and a l-stmulus acquston condton. On each tral n the 2-stmul condton, the postve (correct) and negatve (ncorrect) stmul were presented sde by sde and the anmal chose one by touchng t; f the choce was correct, a food reward was dspensed. On each tral n the 1 -stmulus condton, ether the postve or the negatve stmulus was presented alone; f the stmulus was the postve, t was followed by reward delvery, regardless of the anmal s response to t, and f t was the negatve, t was not followed by reward delvery. Thus, reward delvery was contngent upon the anmal s response to the stmul n the P-stmul condton but not n the l-stmulus condton. The effect of acquston trals under these 2 condtons was measured, n both condtons, by the anmal s subsequent choce when presented wth the 2 stmul sde by sde. Followng preoperatve tranng n ths task, the anmals were frst subjected to unlateral ablaton of the nferotemporal cortex. Ths operaton had lttle effect on the anmals learnng ablty. Then, the amygdala was ablated n the hemsphere contralateral to that n whch the unlateral nferotemporal ablaton had been carred out. Ths combnaton of crossed unlateral lesons of the amygdala and of the nferotemporal cortex, whch dsconnects the amygdala from the output of vsual assocaton cortex, produced a profound mparment n stmulusreward-assocatve learnng. The severty of mparment was equal n the 2 acquston condtons. These results contrast wth those of a prevous experment on the ablty to assocate vsual stmul wth an audtory secondary renforcer, not wth food reward. The amygdala has a specfc role n the learnng of assocatons wth prmary reward, both when those assocatons are response-contngent and when they are not. Blateral amygdalectomy n monkeys has sometmes, but not always, been reported to mpar vsual dscrmnaton learnng that s motvated by food reward. Revewng ths contradctory lterature, GaKan and Harrson (1987) ponted out that the ds- Receved May 19, 1987; revsed Dec. 15, 1987; accepted Dec. 15, Ths research was supported by the Medcal Research Councl. Correspondence should be addressed to ether E. A. Gaffan, Department of Psychology, Readng Unversty, Whteknghts, Readng RG6 2AL, England; or D. Gaffan, Department of Expermental Psychology, South Parks Road, Oxford OX1 3UD, England. Copyrght Socety for Neuroscence /88/ %02.00/O crmnatve stmul n a learnng task mght be assocated wth a varety of dfferent types of attrbute of the reward event. When the postve dscrmnatve stmulus s pared wth a prmary renforcer such as a peanut, for example, the stmulus mght be assocated ether wth the ntrnscally rewardng attrbutes of the peanut, such as ts taste, or wth attrbutes of the peanut that are not ntrnscally rewardng, such as ts vsual appearance. To nvestgate the role of the amygdala n learnng about dfferent attrbutes of the reward event, Gaffan and Harrson (1987) examned a task n whch the reward event that sustaned wthn-problem vsual dscrmnaton learnng was an audtory secondary renforcer. n that task, the audtory secondary renforcer was assocated wth the delvery of a prmary food renforcer, but the vsual dscrmnanda were assocated only wth the audtory renforcer and not wth food. Thus, the vsual stmul were not assocated wth the ntrnscally rewardng attrbutes of food; nstead, they were assocated wth an audtory stmulus that had acqured an extrnsc reward value by vrtue of ts own assocaton wth the ntrnscally rewardng attrbutes of food. Gaffan and Harrson compared the effects on ths task of dsconnectng the amygdala ether from vsual assocaton cortex or from audtory assocaton cortex. These dsconnectons were accomplshed by crossed unlateral lesons of the amygdala n one hemsphere and of assocaton cortex n the opposte hemsphere, and by forebran commssurotomy. Dsconnecton of the amygdala from the audtory modalty produced a profound mparment n the learnng task, but dsconnecton of the amygdala from the vsual modalty left learnng unmpared. The hypothess was put forward that the amygdala s nvolved n assocatng stmul wth the ntrnscally renforcng attrbutes of reward events, and not n assocatng stmul wth the attrbutes that are ntrnscally motvatonally neutral. The present experment was desgned as a further test of ths hypothess and as an nvestgaton of an alternatve nterpretaton of Gaffan and Harrson s (1987) fndngs. One smple predcton from Gaffan and Harrson s hypothess s that dsconnecton of the amygdala from the vsual modalty should mpar vsual dscrmnaton learnng n tasks where the vsual dscrmnatve stmul are assocated wth food reward. Therefore, n the present experment we used the same apparatus and the same dscrmnatve stmul as n Gaffan and Harrson s experment, but the postve dscrmnanda were assocated wth food, rather than wth a secondary renforcer. We dsconnected the amygdala from vsual assocaton cortex n the same way as n the earler study, by crossed unlateral lesons of the vsual assocaton cortex n one hemsphere and of the amygdala n the opposte hemsphere. The predcton from the hypothess outlned above was that ths dsconnecton should produce an

2 The Journal of Neuroscence, September 1988, 8(9) 3145 mparment n the present task, although t produced no mparment n Gaffan and Harrson s (1987) task. The present task was also desgned to test an alternatve nterpretaton of Gaffan and Harrson s (1987) fndngs. n ther task, the assocaton between the audtory secondary renforcer and the food reward was not contngent upon the anmal s behavor. The audtory secondary renforcer was followed by the delvery of food on some trals, accordng to the schedule descrbed n detal by Gaffan and Harrson, but the delvery of food was not determned by the anmal s behavor n the presence of the audtory secondary renforcer. By contrast, the assocatons between the postve vsual dscrmnanda and the audtory secondary renforcer n ther task depended on the anmal s behavor n the presence of the vsual stmul: The postve and negatve vsual stmul n any dscrmnaton problem n ther task were presented sde by sde, and only f the anmal chose the postve stmulus by touchng t was the secondary renforcer produced. Thus, the assocatons between the vsual dscrmnanda and the audtory secondary renforcer were response-contngent, but the assocaton between the audtory secondary renforcer and food was not. t s possble that ths dfference underlay the leson effects that Gaffan and Harrson observed; for example, t s possble that the amygdala s selectvely nvolved n nterstmulus assocatve learnng, and not n nstrumental learnng of assocatons that are contngent upon the anmal s behavor. Therefore, the present experment examned acquston of stmulus-food assocatons under 2 condtons: one n whch the stmulus-food assocatons were response-contngent, and one n whch they were not. The 2 acquston condtons n the present experment, one that s response-contngent and the other not, are 2-stmul and 1 -stmulus acquston condtons. n the 2-stmul acquston condton, the postve and negatve vsual dscrmnatve stmul are presented sde by sde; the anmal chooses one by touchng t, and f the chosen stmulus s the postve stmulus, a food reward s dspensed. Thus, the relaton between the postve vsual stmulus and the food n ths condton of the present task s dentcal to the relaton between the postve vsual stmulus and the audtory secondary renforcer n Gaffan and Harrson s (1987) task. n the 1 -stmulus condton, the anmal produces a sngle vsual stmulus by touchng the screen on whch stmul are dsplayed. Whether the stmulus produced s the postve or the negatve s determned at random. f t s the postve, t s followed by food reward. But the delvery of food n ths condton s ndependent of the anmal s behavor n the presence of the dscrmnatve stmul. Thus, the relaton between the postve vsual stmulus and the food n ths acquston condton s smlar to the relaton between the audtory secondary renforcer and food n Gaffan and Harrson s (1987) task. Followng each of these acquston condtons, stmulus-reward assocaton was assessed by the anmal s choce between the postve and negatve stmul. Ths retenton test s operatonally dentcal to the 2-stmul acquston condton. n effect, therefore, the anmal s gven a seres of 2-choce vsual dscrmnatons, and some of them are preceded by l-stmulus acquston trals n whch the stmulus-reward contngency s ndependent of the anmal s behavor. The number of such l-stmulus acquston trals vares from problem to problem. By examnng the effects of varyng numbers of l-stmulus acquston trals upon the anmal s subsequent choce between the stmul, one can derve a learnng curve for the acquston of stmulus-reward assocatons n the l-stmulus acquston condton and compare t wth the learnng curve n the 2-stmul acquston condton. n ths task we also recorded the anmal s behavor n response to sngle stmul n the l-stmulus acquston condton. As explaned, ths behavor was wthout effect, But t was expected that some responses to the sngle stmul would be made through autoshapng and superstton (Gamzu and Schwam, 1974). Followng preoperatve tranng n ths task, the nferotemporal area was ablated unlaterally and the anmals were retested to confrm that the unlateral ablaton had lttle effect by tself. Then, the amygdala was ablated unlaterally n the hemsphere contralateral to the nferotemporal ablaton. The nferotemporal ablaton was the same as that studed by Gaffan and Harrson (1987). Ths ablaton ncludes unlaterally a cortcal ablaton that, f made blaterally, produces a severe mparment n vsual assocatve learnng for food reward wth the present stmulus materal (D. Gaffan et al., 1986; E. A. Gaffan et al., 1986). Materals and Methods Subjects. Three male cynomolgus monkeys (A4ucacafascculurs) took part n the experment. At the begnnng of preoperatve tranng, as descrbed below, they were expermentally nave. At the tme of the frst surgery, ther average weght was 4.8 kg. Surgery. There were 2 stages of surgery, the frst to ablate the nferotemporal area unlaterally and the second to ablate the amygdala unlaterally. The anesthetc and aseptc methods were as descrbed prevously (Gaffan et al., 1984). After each stage of surgery, d were allowed for recovery before tranng resumed. The unlateral nferotemporal removal was carred out n an dentcal manner to that n parallel experments on vsual dsconnecton (Gaffan and Harrson, 1987,1988). The zygoma was removed and a cranotomy was opened wth drll and rongeurs. The dura was cut n a Y shape over the ntended area of the ablaton, and was sewn afterwards. The ablaton was carred out by cauterzaton and aspraton, wth a 19-gauge metal asprator nsulated except at the tp. t ncluded the nferor bank of the superor temporal sulcus, the lateral bank ofthe occptotemporal sulcus, and all the cortex between those 2 lmts. The parahppocampal gyms, medal to the occptotemporal sulcus, was left ntact. Anterorly, the ablaton was contnued to the tp of the superor temporal sulcus, and the medal boundary n the anteror extent of the leson was a contnuaton of the lne of the occptotemporal sulcus. Posterorly, the ablaton was extended nto the anteror bank of the lunate sulcus, and was lmted by the level of the posteror tp of the lateral sulcusuperorly (although the ablaton dd not nclude the lateral sulcus, beng bounded stll by the nferor bank of the superor temporal sulcus). Both banks of the ascendng tp of the nferor occptal sulcus were ncluded n the posteror part of the ablaton, as were both banks of the anteror mddle temporal sulcus n the anteror part. The amygdalectomy was carred out n the same way as n the experment of Gaffan and Harrson (1987). A cranotomy was opened over the frontal lobe and was extended wth rongeurs anterorly to the brow, medally wthn 2-3 mm of the mdlne, posterorly to the level of the arcuate sulcus, and laterally and nferorly nto the lateral wall of the temporal fossa to the level of the superor temporal sulcus. The dura was cut along the superor, posteror, and nferor margns ofthe cranotomy, and turned back n a flap over the orbt and brow. The frontal lobe was gently retracted wth a bran spoon to expose the medal surface of the anteror part of the temporalobe. A 20-gauge metal asprator that was nsulated except at the tp was used to cauterze and remove a patch of pa mater, 2-3 mm wde, on the medal surface of the temporal lobe superor and posteror to the tp of the rhnal sulcus. The amygdala was then ablated through the defect n the pa mater by aspraton wth the same metal asprator. The lateral ventrcle and the anteror surface of the hppocampus were vsble posteror lmts of the leson. Laterally, gray matter of the amygdala was removed untl whte matter of the temporal stalk and uncnate fasccle appeared. nferorly and anterorly, the ntenton was to leave perrhnal and polar cortex ntact, as far as possble. The dura was sewn and the wound was closed n layers. Hstology. The anmals were gven a lethal dose of anesthetc and then perfused through the heart wth salne, followed by Formal-salne

3 3146 Gaffan et al. l Amygdala and Assocaton wth Reward soluton. The brans were blocked n the coronal stereotaxc plane posteror to the lunate sulcus and were then removed from the head, photographed, and allowed to snk n a sucrose formaln soluton. The brans were cut n 50 Km sectons on a freezng mcrotome. Every ffth secton was retaned and staned wth cresyl volet. Apparatus and stmul. The computer-controlled apparatus, descrbed n detal by Gaffan et al. (1984), dsplayed complex patterns sngly or n pars aganst a plan gray background on a televson that the monkeys vewed through a glass screen. The stmul were presented ether n the center of the screen or 90 mm to the left or rght of center. nfrared beams crossng the surface of the glass screen served to detect the anmals touchng the stmul. Each of the 2 vsual stmul that consttuted a dscrmnaton problem was made of a small shape supermposed on a larger shape (approxmate heghts, 20 and 40 mm, respectvely). Each of the shapes was taken at random from a predefned set of 127 symbols, and was dsplayed n a color chosen at random from 255 possbltes. The random number generator that determned stmul for each problem and left-rght poston at every tral was seeded wth the sesson number, so the stmulus sequence was unque to each sesson but the same, n a gven numbered sesson, for all monkeys. Rewards, consstng of halved blanched peanuts or sugar-coated grans of puffed rce, were dspensed nto a bowl just n front of the lower edge of the screen; the automatc dspenser made a 0.35 set buzz when t operated. The only vsble llumnaton n the expermental cubcle came from the televson screen, but an nfrared floodlght allowed the monkey to be watched over closed-crcut tclcvson. Preoperatve tranng. Before tranng n the man task as descrbed below, the anmals were ntally traned as follows: Prelmnary shapng to touch stmul on the screen was accomplshed by the schedules descrbed n detal by Gaffan et al. (1984). The subjects then had sessons of 2-choce vsual dscrmnaton tranng for mmedate food reward. A new par of stmul, S+ and S -, was generated for each dscrmnaton problem. For each tral wthn a problem, ether S+ was dsplayed on the left and S- on the rght, or vce versa. The stmul remaned on the screen untl the anmal touched one. f t was S+, a food reward was dspensed. When the anmal touched one stmulus, the stmulus that t had not touched dsappeared from the screen; the touched stmulus dsappeared 0.5 set after t had been touched. An ntertral nterval, durng whch the screen was blank gray, then commenced, and the next tral began when 8 set had elapsed wthout the screen s beng touched. For all anmals, each of the last 10 sessons of ths stage of tranng conssted of 5 new dscrmnaton problems presented successvely for 20 trals each. Then, all anmals had 13 sessons of tranng n a task that was almost dentcal to the man task descrbed below. Fnally, preoperatve tranng was completed wth 20 sessons of tranng n the man task, exactly as descrbed below. Man task. n every sesson there were 8 successvely presented dscrmnaton problems, each havng a newly chosen S+ and S-. S+ and S- mght be dsplayed ether smultaneously n the left and rght postons, wth the choce of S+ beng rewarded, or sngly n the center poston, n whch case S+ was termnated by reward delvery and S- was not, regardless of the anmal s response. These are the 2-stmul and l-stmulus trals descrbed n detal below. Every problem was presented for a total of 14 trals. There were 4 possble sequences of trals wthn a problem: (1) fourteen 2-stmul trals, (2) two 1 -stmulus trals followed by twelve 2-stmul trals, (3) four l-stmulus trals followed by ten 2-stmul trals, and (4) eght l-stmulus trals followed by sx 2-stmul trals. Each of these seauences was followed n 2 of the 8 problems, chosen at random, n each sesson. For the l-stmulus trals, ether S+ or S- was presented at random. For the 2-stmul trals, S+ was ether on the left or on the rght at random. Each l-stmulus tral commenced wth an observng stmulus, a whte vertcal lne 24 mm long at the center of the screen. As soon as the monkey touched the observng stmulus, t was replaced by the scheduled dscrmnatve stmulus, S+ or S-, whch remaned on the screen for 3.5 sec. f t was S+, food was delvered 0.5 set before the stmulus ended, but f S-, no food was delvered. n ether case, the termnaton of the stmulus was followed by a 5 set ntertral nterval, durng whch the screen was gray, and any response postponed the next tral for a further 5 sec. The anmal s responses to a sngly presented S+ and S- had no effect, but were counted durng the frst 3 set of each stmulus (except for the frst 0.04 set after the observng stmulus dsappeared, when any beam nterrupton was assumed to be the resdue of the observng response). The crteron of a response was at least 0.02 set contnuous nterrupton of the beams at the center of the screen. Then, for one more response to be accumulated, there frst had to be at least 0.02 set durng whch the beams were unnterrupted. The cumulatve duraton of beam n- terrupton was also recorded for each tral. For each 2-stmul tral wthn a problem, ether S+ was dsplayed on the left and S- on the rght, or vce versa. The stmul remaned on the screen untl the anmal touched one. f the stmulus touched was S+, a food reward was mmedately dspensed. As soon as the anmal touched one stmulus, both stmul dsappeared from the screen. An ntertral nterval, durng whch the screen was blank gray, then commenced, and the next tral began when 8 set had elapsed wthout the screen s beng touched. Procedure. Followng ntal preoperatve tranng as descrbed above, 20 sessons of tranng n the man task completed preoperatve tranng. The nferotemporal cortex was then ablated unlaterally, and 20 further sessons of tranng n the man task were gven. The amygdala was then ablated n the hemsphere contralateral to the nferotemporal ablaton, and 20 further sessons of tranng n the man task completed the experment. Results Hstologcal Mcroscopc examnaton of each bran showed that the lesons were as ntended (see Materals and Methods). The ablaton of vsual assocaton cortex n the hemsphere contralateral to the amygdalectomy was very smlar n all 3 monkeys, and was the same as n our prevous experment wth ths leson (see Fgs. l-3 n Gaffan and Harrson, 1987). Ths leson ncluded the lateral bank of the occptotemporal sulcus and the nferor bank of the superor temporal sulcus, but left the superor temporal gyrus and the parahppocampal gyrus ntact. Anterorly, as llustrated n Fgure 1, the leson ncluded both banks of the anteror mddle temporal sulcus, but left ntact the cortex medal to the anteror mddle temporal sulcus. Fgure 1 also llustrates the amygdalectomy, n the hemsphere contralateral to the ablaton of vsual assocaton cortex. t can be seen that the amygdalectomy was complete except for some parts of the posteror dorsal amygdalod complex. The other 2 monkeys were smlar to the monkey llustrated. Monkey XVA-3 was chosen for llustraton (Fg. 1) because ths was the monkey wth the worst postoperatve performance (Table 1); ths bran can be compared wth the bran of the ndvdual monkey llustrated n an earler report (see Fg. 1 n Gaffan and Harrson, 1987) that showed the best postoperatve performance n the earler experment. Comparson ndcates that the dfference between the unmpared performance n the earler experment and the severe defct n the present experment cannot be ascrbed to any obvous varaton n the extent of the ablatons. Mcroscopc examnaton and comparson of the 6 brans from the 2 experments confrmed ths concluson. Choces n 2-stmul trals As explaned n the ntroducton, 2-stmul trals played 2 roles n the present task, namely, as one of the acquston condtons for stmulus-reward assocatons, and as a test for the retenton of those assocatons from prevous acquston trals. Table 1 shows the accuracy of choce n 2-stmul trals as a functon of the precedng acquston trals, themselves ether 1 -stmulus or 2-stmul trals. As descrbed above (see Man task n Materals and Methods),, new dscrmnaton problems had tral seauences 1-m ~~~ of 4 possble types: (1) fourteen 2-stmul trals, (2) two 1 -stmulus trals followed by twelve 2-stmul trals, (3) four 1 -stmulus trals followed by ten 2-stmul trals, and (4) eght l-stmulus trals followed by sx 2-stmul trals. To explan the dervaton

4 The Journal of Neuroscence, September 1988, f?(9) 3147

5 3148 Gaffan et al. - Amygdala and Assocaton wth Reward PRE (unlateral T only) POST dsconnecton 60 No. of precedng sngle stmulus presentatons e-* 4! C--r 6 c Trals Fgure 2. Group learnng curves followng unlateral nferotemporal ablaton (left) and the addton of amygdalectomy n the hemsphere contralateral to the nferotemporal ablaton (rght). The 4 curves n each panel represent performance at choce trals n 4 types of problem, each havng a dfferent number of 1 -stmulus acquston trals precedng the 2-stmul choce trals. of the numbers n Table 1, consder the 6 numbers that represent monkey XVA-l s preoperatve performance. The top row (75.0, 87.5, loo.o), representng performance after two, four, and eght 1 -stmulus acquston trals, s the percentage of correct choces on tral 3 of type 2 problems, tral 5 of type 3 problems, and tral 9 of type 4 problems, respectvely. The bottom row (85.0, 90.0, loo.o), representng performance after two, four, and eght 2-stmul acquston trals, s the percentage of correct choces on trals 3, 5, and 9 of type 1 problems. Table 1 shows that the anmals ncreasngly tended to choose S-- n 2-stmul trals as the number of precedng acquston trals ncreased. The effect of l-stmulus acquston trals was almost equal to the effect of 2-stmul acquston trals. The effects of surgery were straghtforward. The frst stage, unlateral removal of the nferotemporal cortex, produced lttle change n performance of the task. The dsconnecton resulted n a severe dsrupton that appeared to affect learnng from sngle and choce trals to a smlar degree. Ths s llustrated n more detal n Fgure 2, whch shows tral-by-tral learnng curves from the 4 types of problem, averaged across subjects, n the last 2 phases of the experment. On nspecton, t appears that, followng dsconnecton, the anmals contnued to show some learnng from both sngle and choce trals, and to a smlar extent from each, but at a strkngly lower level than before. Statstcal analyss, appled to the data of Table 1, confrmed these mpressons. Takng all three phases of the experment together, there was a sgnfcant ncrease n correct choces as the number of precedng acquston trals ncreased from 2 to Table 1. Percentage of correct choces of S+ after 2 learnng condtons Surgcal stage of the experment Preoperatve Unlat. T Dsconnecton (no. of acquston (no. of acquston (no. of acquston trals) trals) trals) Monkev Condton XVA- 1 XVA-2 XVA-3 Average 1 -stmulus stmul stmulus stmul stmulus stmul stmulus stmul Chance level s 50% and the maxmum s 100%.

6 The Journal of Neuroscence, September 1988,8(g) 3149 Table 2. Frequency per tral of touchng stmul n l-stmulus trals 100 Surgcal stage of the experment Monkey Stmulus Pre- Dsconoperatve Unlat. T necton XVA- 1 s S XVA-2 s S XVA-3 s S s l l Group Means cl Pre -0p ndvdual scores 8 (F = 16.32, dfl2,4); p < 0.05). Also, there were sgnfcantly more correct choces followng 2-stmul acquston trals than after 1 -stmulus acquston trals (F = , df( 1,2); p < 0.0 1). But the effects of the number of acquston trals (2, 4, and 8) and of the type of tral ( 1 -stmulus and 2-stmul) dd not nteract wth each other (F c 1). There was a sgnfcant dfference n overall performance across the three surgcal stages of the experment (F = 31.54, &2,4); p < 0.01). Planned comparsons ndcated that the small drop n average performance after the unlateral nferotemporal leson dd not reach statstcal sgnfcance (F = 2.16, dfl1,4); p > 0.05), but the further deteroraton followng the addton of the amygdala ablaton was hghly sgnfcant (F = 31.54, dfll,4); p < 0.01). There was no evdence that ths effect of dsconnecton appled dfferentally to learnng from l-stmulus and from 2-stmul trals: The nteracton between the effect of the 3 surgcal stages and the effect of the 2 types of acquston tral was not sgnfcant (F < 1). The nteracton between the stages of surgery and the number of precedng trals (2, 4, or 8) approached sgnfcance (F = 0.05 < p < O.lO), reflectng the flattenng of the learnng curves n the fnal stage. Comparson wth audtory secondary renforcement One of the man purposes of the present experment, as explaned n the ntroducton, was to compare the present task wth the task of Gaffan and Harrson (1987), whch requred assocaton of vsual stmul wth an audtory secondary renforcer, rather than wth food. n both experments, the anmals were tested both as normal anmals preoperatvely and followng dsconnecton. n the earler experment, learnng was assessed by performance on tral 4 of dscrmnaton problems; as explaned n the earler paper, there was a specal reason, n the desgn of the task, for the selecton ofths measure. Furthermore, to allow for the possblty of recovery wth practce, the leson effects n the earler experment were assessed from the fnal 5 sessons of the 20 sessons of tranng that followed each surgcal stage of the experment. Therefore, to compare the present results wth the earler results, we computed perormance on tral 4 of dscrmnaton problems n the last 5 sessons of the preoperatve tranng and n the last 5 sessons of the tranng that followed dsconnecton. (Ths measure s an average of tral 4 performances n problems wth tral sequences numbered 1 and 2 n Materals and Methods; these are the problems n whch tral 4 was a 2-stmul choce tral.) The comparson s shown n Fgure 3. The effect of the dsconnecton was qute dfferent n the 2 tasks, as confrmed by a sgnfcant nteracton, n the data n Fgure 3, between dsconnecton (Pre-op vs Post-op) and the tasks (F = 42.59, dfl1,4); p < 0.01). Prmary Renforcement Audtory Secondary Renforcement Fgure 3. A comparson of the present experment (left) wth that of Gaffan and Harrson (1987; rght). Both experments examned the effect of dsconnectng the amygclala from vsual assocaton cdrtex on vsual dscrmnaton learnng. n the present experment, the vsual stmul were assocated wth food reward, but n the earler expermenthey were assocated wth an audtory secondary renforcer. As an ndcaton of the effcency of learnng, the graph shows the percentage of correct choces on tral 4 of the vsual dscrmnaton problems. The same anmals were tested when normal (Be-op) and after dsconnecton surgery (Post-o&. The bars show group averages and the lnes show ndvdual anmals. Responses durng l-stmulus trals Behavor durng the 1 -stmulus presentatons themselves, as dstnct from the effect of those trals upon subsequent 2-stmul choce trals, was assessed by countng the number of tmes the anmal touched the stmulus and by accumulatng the total tme spent n contact wth the stmulus. These 2 measures gave smlar pctures. Table 2 presents the number of touches, and shows the mean number of responses to all presentatons of S+ and S-, except the frst n each problem (when dfferentaton was of course mpossble), pooled over problem types 2-4 across the 3 surgcal stages of the experment. Two anmals showed lttle or no sgn of respondng dfferently to S + and S -, and one of them rarely touched ether. One monkey, No. XVA- 1, touched the S+ stmul more than the S- stmul; ths monkey contnued to show some dscrmnaton n the number of touches followng the dsconnecton surgery. Ths was also the ndvdual,anmal that showed the best overall performance n choce trals at all stages (Table 1). The consstent effect of the surgery on choce trals n all 3 subjects (Table 1, Fg. 3), despte the subjects wdely varyng response rates durng the 1 -stmulus trals (Table 2) suggests that assocatve learnng durng the 1 -stmulus trals was ndependent of overt responses to the stmul durng the l-stmulus trals. Dscusson The experment had 3 man purposes. The frst was to test the hypothess that dsconnecton of the nferotemporal area from the amygdala would mpar monkeys learnng of assocatons between vsual stmul and food rewards. Ths hypothess was confrmed. The second was to compare the effects of the dsconnecton upon stmulus-reward-assocatve learnng under 2 acquston condtons, one contngent upon the anmals choces

7 3150 Gaffan et al. - Amygdala and Assocaton wth Reward and the other not. These 2 acquston condtons were almost equally effectve n normal anmals, and were equally affected by dsconnecton. Thus we conclude that the amygdala partcpates n stmulus-reward-assocatve learnng both when the anmal chooses a vsual stmulus by touchng t and when a vsual stmulus sgnals reward ndependently of the anmal s behavor n response to that stmulus. The thrd purpose was to draw a comparson between the effects of dsconnecton upon learnng of assocatons wth food and ts effects upon learnng of assocatons wth an audtory secondary renforcer, as establshed n an earler experment (Gaffan and Harrson, 1987). The severe mparment n the present experment, wth prmary food rcnforcemcnt, contrasted sharply wth the abscncc of mparment n the prevous experment, wth audtory secondary renforcement. Ths contrast s further sharpened by some dfferences n the surgcal operatons n the 2 experments. Gaffan and Harrson (1987) ablated both the nferotemporal area unlaterally and the amygdala contralateral to the nferotemporal ablaton n one operaton; these 2 ablatons were carred out n 2 stages of surgery n the present experment. Snce one-stage surgery n general produces a greater mparment than multplestage surgery (Fnger, 1978), ths dfference s unlkely to explan the contrastng behavoral results. Further, Gaffan and Harrson s (1987) anmals remaned unmpared when the forebran commssures and the fomx-fmbra were transected, the mparment n the present experment was manfest n anmals wth the forebran commssures and the hppocampal system ntact. For these reasons, the dfference between the effects of dsconnecton n the 2 experments can be ascrbed to the dfference n the tasks. There are several sources of evdence n favor of the hypothess (outlned n the ntroducton) that the amygdala s nvolved n assocatng stmul wth the ntrnsc reward value of food. One s the well-establshed effects of amygdalectomy on oral behavor. The observaton that amygdalectomzed monkeys frequently take nedble objects nto ther mouths (Weskrantz, 1956; Horel and Keatng, 1969, 1972) s consstent wth the hypothess that the operaton has mpared the assocaton of the vsual appearance of objects wth ther reward value as food. Evdence also comes from the reports that blateral amygdalectomy retards vsual dscrmnaton learnng for food reward, these reports, by Schwartzbaum and Poulos (1965) and others, were dscussed n some detal by Gaffan and Harrson (1987). A thrd source of evdence s the experment of Gaffan and Harrson (1987); the present experment strengthens that evdence by rulng out an alternatve nterpretaton of ther fndngs n terms of response contngency, as explaned n the ntroducton. The effect of the crossed unlateral lesons of the amygdala and the nferotemporal cortex, n the present experment, s to dsconnect the normal drect nteracton between those 2 structures: Followng the unlateral lesons, one nferotemporal area remans ntact and one amygdala remans ntact, but the drect projecton from the nferotemporal area to the amygdala (Herzog and Van Hoesen, 1976) s dsrupted blaterally by destructon of ts orgn n one hemsphere and destructon of ts termnaton n the other. n earler work on the nferotemporal area (D. Gaffan et al., 1986; E. A. Gaffan et al., 1986), we argued that the nferotemporal area provdes an nput to a memory system of assocatons wth food reward. t s therefore an attractve hypothess that the acquston of assocatons between vsual stmul and the reward value of food depends upon a modfcaton n the amygdala of the cells that receve the projecton from the nferotemporal area. References Fnger, S. (ed.) (1978) Recovery from Bran Damage: Research and Theory, Plenum, New York. Gaffan, D., and S. Harrson (1987) Amygdalectomy and dsconnecton n vsual learnng for audtory secondary renforcement by monkeys. J. Neurosc. 7: Gaffan, D., and S. Harrson (1988) nferotemporal-frontal dsconnecton and fomx transecton n vsuo-motor condtonal learnng by monkeys. Behav. Bran Res. (n press). Gaffan, D., R. C. Saunders, E. A. Gaffan, S. Harrson, C. Shelds, and M. J. Owen (1984) Effects of fomx transecton upon assocatve memory n monkeys: Role of the hppocampus n learned acton. Q. J. Exp. Psychol. 36B: Gaffan, D., S. Harrson, and E. A. Gaffan (1986) Vsual dentfcaton followng nferotemporal ablaton n the monkey. Q. J. Exp. Psychol. 38B: Gaffan, E. A., S. Harrson, and D. Gaffan (1986) Sngle and concurrent dscrmnaton learnng by monkeys after lesons of nferotemporal cortex. Q. J. Exp. Psychol. 388: Gamzu, E., and E. Schwam (1974) Autoshapng and automantenance of a keypress response n squrrel monkeys. J. Exp. Anal. Behav. 21: Herzog, A. G., and G. W. Van Hoesen (1976) Temporal neocortcal afferent connectons to the amygdala n the rhesus monkey. Bran Res. 115: Horel, J. A., and E. G. Keatng (1969) Partal Kluver-Bucy syndrome produced by cortcal dsconnecton. Bran Res. 16: Horel, J. A., and E. G. Keatng (1972) Recovery from a partal Kluver- Bucy syndrome n the monkey produced by dsconnecton. J. Comp. Physol. Psychol. 79: Schwartzbaum, J. S., and D. A. Poulos (1965) Dscrmnaton behavor after amygdalectomy n monkeys: Learnng set and dscrmnaton reversal. J. Comp. Physol. Psychol. 60: Weskrantz, L. (1956) Behavoral changes assocated wth ablaton of the amygdalod complex n monkeys. J. Comp. Physol. Psychol. 49: