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Amygdalar Interaction with the Mediodorsal Nucleus of the Thalamus and the Ventromedial Prefrontal Cortex in Stimulus-Reward Associative Learning in the Monkey

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Amygdalar Interaction with the Mediodorsal Nucleus of the Thalamus and the Ventromedial Prefrontal Cortex in Stimulus-Reward Associative Learning in the Monkey The Journal of Neuroscience, November 1990, fO(11): 3479-3493 Amygdalar Interaction with the Mediodorsal Nucleus of the Thalamus and the Ventromedial Prefrontal Cortex in Stimulus-Reward Associative Learning in the Monkey David Gaffan’ and Elisabeth A. Murray* ‘Department of Experimental Psychology, Oxford University, Oxford OX1 3UD, England, and *Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Maryland 20892 Cynomolgus monkeys (Macaca fascicularis) were assessed One kind of associative learning in which the amygdala is of for their ability to associate visual stimuli with food reward. central importance is the associationof a sensorystimulus with They learned a series of new 2-choice visual discriminations the incentive value of food reward. In visual-discrimination between colored patterns displayed on a monitor screen. learning for food reward, the role of the amygdala varies ac- The feedback for correct choice was the delivery of food. In cording to the associative structure of the task. If visual dis- order to promote associative learning between the visual criminative stimuli are associateddirectly with the incentive stimuli and the incentive value of the food reward, reward value of the food reward, efficient learning dependson an in- delivery was not accompanied by any distinctive visual feed- trahemispheric interaction between the amygdala and the vi- back on the display screen. The rate of learning new prob- sual-associationcortex ipsilateral to it (E. A. Gaffan et al., 1988). lems was assessed before and after surgery in a total of 16 But when visual discriminative stimuli are associatedwith the monkeys. Three groups of 3 monkeys received bilaterally incentive value indirectly, via the mediation of a direct asso- symmetrical ablations in either the amygdala, the medio- ciation with an auditory or visual secondary reinforcer, visual dorsal nucleus of the thalamus, or the ventromedial pre- interaction with the amygdala is less important (Gaffan and frontal cortex. All these groups showed a severe postop- Harrison, 1987; Gaffan et al., 1989). erative learning impairment. Seven other animals were given In the presentexperiment, we examined a task in which visual a unilateral ablation in 1 of those 3 structures and a second discriminative stimuli are associateddirectly with the incentive unilateral ablation, in each case contralateral to and different value of the food reward. Our aim was to determine which from the first, in order to produce 2 groups in which a putative structures, apart from the visual-associationcortex, the amyg- amygdalo-thalamo-prefrontal pathway had been discon- dala interacts with in this task. E. A. Gaffan et al. (1988) showed nected by crossed unilateral lesions. One disconnection that this type of learning is severely impaired by crosseduni- group had lesions in the amygdala and ventromedial pre- lateral lesions of the amygdala in one hemisphere and of the frontal cortex; the other had lesions in the amygdala and the visual-association cortex in the other hemisphere. This com- mediodorsal nucleus of the thalamus. The disconnection bination of lesions disconnects the intrahemispheric pathway groups showed a significant impairment, but the effect of from the visual-associationcortex to the amygdalaby destroying the disconnection surgeries was significantly milder than the its origin in one hemisphere and its destination in the other. effect of any of the 3 bilaterally symmetrical lesions. There- The results suggestedthat visual information and incentive- fore, symmetrical bilateral lesions in either the amygdala, value information converge in the amygdala and are associated the mediodorsal nucleus, or the ventromedial prefrontal cor- together there. If so, then the product of this associativeprocess tex produce similar impairments in the present task, implying (the information, retrieved from memory, that a certain visual that these structures are functionally related to each other; stimulus has been paired in the past with food) needs to be but the relatively mild effect of disconnecting these struc- relayed to further projection targets in order to elicit ultimately tures from each other argues against the hypothesis that a motor response,namely, an instrumental discriminative re- they are serial stages in a single, tightly linked functional sponseto that stimulus. Possiblestages of this further pathway pathway. can be tested by disconnection experiments. Disconnection of the amygdala from further projection targets in the hypothetical pathway should disrupt the present type of visual associative- learning task in the same way as does disconnection of the Received Jan. 17, 1990; revised June 6, 1990; accepted June 8, 1990. amygdala from visual-association cortex. The research was supported by the Medical Research Council and by NATO The amygdala and adjacent periallocortical regions send a Grant 0 184/87. We thank S. Watkins for assistance in training the monkeys. Send direct ipsilateral projection to the medial part of the mediodorsal reprint request to either D. Gaffan, Department ofExperimental Psychology, South Parks Road, Oxford OX1 3UD, England, or E. A. Murray, Laboratory of Neu- thalamus (Porrino et al., 1981; Aggleton and Mishkin, 1984; ropsychology, National Institute of Mental Health, Building 9, Room IN-107, Russchenet al., 1987; Gower, 1989). The medial part of the Bethesda, MD 20892. Correspondence should be addressed to D. Gaffan, Department of Experimental mediodorsalthalamus, in turn, projects heavily to the ipsilateral Psychology, South Parks Road, Oxford OX1 3UD, England. ventromedial prefrontal cortex (Tobias, 1975; Goldman-Rakic Copyright 0 1990 Society for Neuroscience 0270-6474/90/l 13479-15$03.00/O and Porrino, 1985; Giguere and Goldman-Rakic, 1988). Bache- 3480 Gaffan and Murray * Amygdala-MD-Frontal: Is It a System? valier and Mishkin (1986) have argued from behavioral results VF/A, n = 4) or in the mediodorsal thalamus and the amygdala (group in recognition memory tasks that “the medial temporal, medial MD/A, n = 3). All of the animals in the disconnection groups were first given one unilateral lesion alone and were tested behaviorally after this thalamic and ventromedial prefrontal regions of the brain are first surgery (Post 1) in order to verify that a single unilateral lesion was each apparently part of an integrated memory circuit” (p 260). without effect in the present task. They were then given a seeond lesion, In the present task, therefore, a simple and attractive hypothesis contralateral to the first, and a further behavioral test (Post2) was ad- is that information and control flows from the visual discrim- ministered. All 3 animals in group MD/A had the lesion in the medio- inative stimulus, associated in memory with food reward, to the dorsal thalamus first and the lesion in the amygdala second. Among group VF/A, 2 animals(Dl and D2) had the ventromedialprefrontal instrumental discriminative response along a tightly linked lesionfirst, whilethe other 2 (D3 andD4) had the amygdalalesion first. pathway through the visual-association cortex, amygdala, thal- Finally, groupVF/A wassubjected to forebraincommissurotomy and amus. and prefrontal cortex. If this hvoothesis is true. then weregiven a third behavioraltest (Post3). bilaterally symmetrical lesionsin any ofthese structuresshould Surgical methods. The surgical.opera&ons were carried out under sterileconditions. Barbiturate was infused through an intravenouscan- disrupt this type of learning. Furthermore, crossedunilateral nulaat a rate sufficientto maintaindeep anesthesia. The ablationswere lesionsof the amygdala and ventromedial prefrontal cortex, or madeby aspirationunder visual guidancewith the aid of an operating of the amygdala and mediodorsal thalamus, should disrupt microscope. The tissue was closed in layers with silk sutures. A pro- learning as effectively as bilateral lesionsin each of these struc- phylactic dose of antibiotic was administered at the end of the surgery. tures, becausethey should disconnect the pathway of the flow Postoperative recovery was in all cases uneventful. The surgical method for making amygdala lesions was identical to in the sameway asthe crossedunilateral lesionsof the amygdala that described by Gaffan and Harrison (1987). The medial temporal and visual association cortex did in the experiment by E. A. lobe was exposed by retracting the frontal lobe over the orbit. The pia Gaffan et al. (1988). mater was cauterized in an area approximately 5 mm in diameter on Therefore, we compared the learning disability produced by the medial surface of the temporal lobe medial and superior to the rhinal sulcus. The amygdala and the periamygdaloid cortex medial to the bilateral lesions with the learning disability produced by dis- amygdala were then ablated by aspiration through the defect in the pia connection of the hypothesized pathway. One disconnection mater. White matter of the temporal stem, and the lateral ventricle and group had crossedunilateral lesions of the ventromedial pre- anterior surface of the hippocampus, were visible boundaries of the frontal cortex and the amygdala; in addition, this group was ablation posteriorly, laterally, and inferiorly. subsequently tested, after forebrain commissurotomy, for the To produce an ablation in the ventromedial frontal cortex, a bone flap was raised over the frontal lobe, and the dura mater was cut in a possibility that their residual learning ability was mediated by Y shape to expose the whole
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