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The authors present a brief review of recent evidence, primarily from studies with rats and monkeys, for an important role of the amygdala in processing of positive rewards. The authors contrast amygdala-independent and amygdala-dependent reward processing, emphasizing the role of amygdala in the formation of stimulus value associations in learning about the positive consequences of events.
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Baxter M.G., Murray E.A. The amygdala and reward. Nat Rev Neurosci. 7:2002;563-573 The authors present a brief review of recent evidence, primarily from studies with rats and monkeys, for an important role of the amygdala in processing of positive rewards. The authors contrast amygdala-independent and amygdala-dependent reward processing, emphasizing the role of amygdala in the formation of stimulus value associations in learning about the positive consequences of events.
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Cardinal R.N., Parkinson J.A., Hall J., Everitt B.J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev. 26:2002;321-352 The authors present an extensive review of the contributions of these brain regions to performance in a wide range of learning tasks thought to reveal learning about the affective value of environmental stimuli.
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This is a comprehensive review, which integrates findings from behavioral, brain imaging, neuropsychological and animal studies. The author proposes that different aspects of decision processes are subserved by three major prefrontal regions: the OFC and ventromedial areas, the dorsolateral areas, and the anterior and ventral cingulate areas.
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Krawczyk D.C. Contributions of the prefrontal cortex to the neural basis of human decision making. Neurosci Biobehav Rev. 26:2002;631-664 This is a comprehensive review, which integrates findings from behavioral, brain imaging, neuropsychological and animal studies. The author proposes that different aspects of decision processes are subserved by three major prefrontal regions: the OFC and ventromedial areas, the dorsolateral areas, and the anterior and ventral cingulate areas.
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The authors report three studies that implicate BLA in the coding of specific reinforcing outcomes. Pre-training lesions of the BLA impaired performance on an instrumental devaluation task (sensory-specific satiety), reduced sensitivity to post-training degradation of response-reinforcer contingencies, and were unable to use properties of the reinforcers to guide correct responding in a discrimination task. The authors suggest that BLA is crucial for "relating the sensory features of nutritive commodities to the consequences induced by their consumption".
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Balleine B.W., Killcross A.S., Dickinson A. The effect of lesions of the basolateral amygdala on instrumental conditioning. J Neurosci. 23:2003;666-675 The authors report three studies that implicate BLA in the coding of specific reinforcing outcomes. Pre-training lesions of the BLA impaired performance on an instrumental devaluation task (sensory-specific satiety), reduced sensitivity to post-training degradation of response-reinforcer contingencies, and were unable to use properties of the reinforcers to guide correct responding in a discrimination task. The authors suggest that BLA is crucial for "relating the sensory features of nutritive commodities to the consequences induced by their consumption".
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Rats with BLA lesions failed to show a devaluation in a Pavlovian approach conditioning task, but showed normal devaluation effects in a within-compound taste learning (sensory preconditioning) task. The authors suggest that the BLA is crucial for learning associations between sensory and incentive stimulus attribute cues but not for learning sensory-sensory associations.
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Blundell P., Hall G., Killcross S.L. Preserved sensitivity to outcome value after lesions of the basolateral amygdala. J Neurosci. 23:2003;7702-7709 Rats with BLA lesions failed to show a devaluation in a Pavlovian approach conditioning task, but showed normal devaluation effects in a within-compound taste learning (sensory preconditioning) task. The authors suggest that the BLA is crucial for learning associations between sensory and incentive stimulus attribute cues but not for learning sensory-sensory associations.
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In this event-related fMRI study, participants received visual cues, one paired with the odor of ice cream, one with the odor of peanut butter, and one not paired with any odor. They then were allowed to eat either peanut butter or ice cream to satiation and finally were retested. Both amygdala and OFC responded more to the visual CS-odor pair whose corresponding food item was not devalued by satiation than to the other events. In a follow-up study (Gottfried JA, pers comm), testing in the presence of the visual cues only revealed activation of OFC but not amygdala, consistent with the claim that amygdala is crucial for learning about incentive values of cues but not for guiding behavior based on those cue-outcome expectancies.
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Gottfried J.A., O'Doherty J., Dolan R.J. Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science. 301:2003;1104-1107 In this event-related fMRI study, participants received visual cues, one paired with the odor of ice cream, one with the odor of peanut butter, and one not paired with any odor. They then were allowed to eat either peanut butter or ice cream to satiation and finally were retested. Both amygdala and OFC responded more to the visual CS-odor pair whose corresponding food item was not devalued by satiation than to the other events. In a follow-up study (Gottfried JA, pers comm), testing in the presence of the visual cues only revealed activation of OFC but not amygdala, consistent with the claim that amygdala is crucial for learning about incentive values of cues but not for guiding behavior based on those cue-outcome expectancies.
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Rats were trained in a series of go/no-go discrimination tasks in which responding after one odor was reinforced with sucrose and responding after another odor was reinforced with (aversive) quinine. Although rats with bilateral lesions of the basolateral amygdala and sham lesioned control rats showed comparable behavioral accuracy in the behavioral discrimination task and some similarities in OFC neuronal activity, they showed substantially reduced coding of cue-outcome expectancies. Fewer cue-selective OFC neurons were observed in BLA lesioned rats, and unlike in shams, these neurons did not also code the upcoming reinforcer after a response, but rather were more often bound to cue identity. This last characteristic was especially evident in reversal learning, in which OFC neurons of lesioned rats were more likely to maintain the same cue-selectivity after reversal as in the original training.
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Schoenbaum G., Setlow B., Saddoris M.P., Gallagher M. Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends on output from basolateral amygdala. Neuron. 39:2003;855-867 Rats were trained in a series of go/no-go discrimination tasks in which responding after one odor was reinforced with sucrose and responding after another odor was reinforced with (aversive) quinine. Although rats with bilateral lesions of the basolateral amygdala and sham lesioned control rats showed comparable behavioral accuracy in the behavioral discrimination task and some similarities in OFC neuronal activity, they showed substantially reduced coding of cue-outcome expectancies. Fewer cue-selective OFC neurons were observed in BLA lesioned rats, and unlike in shams, these neurons did not also code the upcoming reinforcer after a response, but rather were more often bound to cue identity. This last characteristic was especially evident in reversal learning, in which OFC neurons of lesioned rats were more likely to maintain the same cue-selectivity after reversal as in the original training.
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••]. The authors recorded from BLA neurons in rats with unilateral excitotoxic or sham lesions of the OFC. Lesioned rats showed changes in neural coding in BLA ipsilateral to the OFC lesion. BLA neurons in lesioned rats were less likely to show outcome-specific responding during the delay interval after responding but before reinforcer delivery than neurons in sham rats. Furthermore, odor cue-selective neurons in lesioned rats were much less likely to reverse their cue selectivity after reversal training than comparable neurons in shams.
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Saddoris, M.P.1
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Schoenbaum G., Setlow B., Nugent S.L., Saddoris M.P., Gallagher M. Lesions of orbitofrontal cortex and basolateral amygdala complex disrupt acquisition of odor-guided discriminations and reversals. Learn Mem. 10:2003;129-140.
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Although Pavlovian conditioned responding of rats with lesions of BLA made before training showed no sensitivity to reinforcer devaluation (see text), rats with BLA lesions made after light-food training but before food devaluation were unimpaired. By contrast, responding of rats with OFC lesions made after light-food pairings was not sensitive to subsequent food devaluation. The authors suggested that BLA is crucial for forming representations linking cues to the incentive properties of outcomes but not for the use of the those representations to guide behavior, which is instead dependent on OFC function.
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Pickens C.P., Saddoris M.P., Setlow B., Gallagher M., Holland P.C., Schoenbaum G. Different roles for orbitofrontal cortex and basolateral amygdala in a reinforcer devaluation task. J Neurosci. 23:2003;11078-11084 Although Pavlovian conditioned responding of rats with lesions of BLA made before training showed no sensitivity to reinforcer devaluation (see text), rats with BLA lesions made after light-food training but before food devaluation were unimpaired. By contrast, responding of rats with OFC lesions made after light-food pairings was not sensitive to subsequent food devaluation. The authors suggested that BLA is crucial for forming representations linking cues to the incentive properties of outcomes but not for the use of the those representations to guide behavior, which is instead dependent on OFC function.
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Pickens CP, Saddoris MP, Gallagher M, Holland PC: Orbitofrontal lesions impair use of cue-outcome associations in a devaluation task [abstract]. Soc Neurosci 2003: 89.13.
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In this event-related fMRI study, pictures of faces were paired or unpaired with pleasant, neutral, or unpleasant odors in classical conditioning procedures. Activity of medial and lateral OFC was associated with presentations of faces that signaled pleasant and unpleasant odors, respectively. Amygdala activity was initially related to presentations of signals for pleasant odors, but that response habituated over testing. Activity of the nucleus accumbens increased with presentations of signals for pleasant odors but decreased with signals for unpleasant odors.
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Gottfried J.A., O'Doherty J., Dolan R.J. Appetitive and aversive olfactory learning in humans studied using event-related functional magnetic resonance imaging. J Neurosci. 15:2002;10829-10837 In this event-related fMRI study, pictures of faces were paired or unpaired with pleasant, neutral, or unpleasant odors in classical conditioning procedures. Activity of medial and lateral OFC was associated with presentations of faces that signaled pleasant and unpleasant odors, respectively. Amygdala activity was initially related to presentations of signals for pleasant odors, but that response habituated over testing. Activity of the nucleus accumbens increased with presentations of signals for pleasant odors but decreased with signals for unpleasant odors.
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Gottfried, J.A.1
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Dissociable contributions of the human amygdala and orbitofrontal cortex to incentive motivation and goal selection
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Arana F.S., Parkinson J.A., Hinton E., Holland A.J., Owen A.M., Roberts A.C. Dissociable contributions of the human amygdala and orbitofrontal cortex to incentive motivation and goal selection. J Neurosci. 29:2003;9632-9638 In this study, food-sated participants were shown restaurant menus that varied in incentive value, based on a prior survey of their food preferences. On half of the trials, the participants were asked to choose from the menus. PET analysis of regional cerebral blood flow showed activation of the amygdala by high-incentive menus, regardless of whether a choice had to be made; that activation was proportional to participants' subjective ratings of menu incentive value. Medial OFC responded to high-incentive menus and on any trials that required a choice response; activation on choice trials was proportional to participants' subjective ratings of choice difficulty. Finally, lateral OFC responded when participants had to choose among similarly desirable alternatives. The authors suggest that amygdala and OFC have specialized roles within a system that underlies the selection of goals based on expectancies of their incentive values. Whereas the amygdala provides magnitude estimates, the OFC "integrate(s) diverse aspects of goal information including value, sensory, experiential and semantic components to guide prospective (expectancy-based) behavior".
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J Neurosci
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Arana, F.S.1
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Holland, A.J.4
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36
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Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices
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O'Doherty J., Critchley H., Deichmann R., Dolan R.J. Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices. J Neurosci. 23:2003;7931-7939 The authors present an fMRI study of normal participants in a two-choice visual discrimination reversal task. In a 'choice' condition, responses to one visual cue yielded a monetary gain 70% of the time and a monetary loss 30% of the time; responses to the other stimulus had the opposite consequences. After a discrimination criterion was met, the discrimination contingencies were reversed. In a response independent condition, participants could not choose their responses, rather reinforcement was determined by the performance of another 'yoked' subject. Outcome-dependent activation of central/medial OFC was found in both choice and response-independent conditions, but was greater in the choice condition. Amygdala and striatal activation to reward versus punishment occurred without regard to choice condition. Finally, enhanced responding of medial and left lateral OFC was observed after both reinforced (correct) and punished (incorrect) trials that were not followed by a change in response on the next trial, relative to the neural response on punished trials that were followed by a subsequent correct response. Thus, this signal reflected a continuing behavioral strategy of response maintenance or persistence rather than the trial outcome alone. The authors conclude that some prefrontal regions "represent valence irrespective of behavioral choice, other regions are sensitive to response maintenance, and other regions are involved in detecting a change in response contingencies".
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J Neurosci
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O'Doherty, J.1
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