Central to many emotional responses is the accompanying peripheral somatic and autonomic arousal, feedback from which has been hypothesized to enhance emotional memory and to contribute to appraisal processes and decision making, and dysfunction of which may contribute to antisocial behaviour. Whilst peripheral arousal may accompany both positive and negative emotional contexts, its relationship with the former is poorly understood, as are the neural mechanisms underlying such a relationship. The purpose of the present study was to determine the autonomic correlates of anticipation, as well as consumption, of high incentive food, in the freely moving common marmoset and to investigate the contribution of the amygdala to such effects. Blood pressure (BP) and heart rate (HR) were measured remotely by a telemetric device implanted into the descending aorta and behavioural responses were monitored whilst marmosets viewed preferred or non-preferred foods and were then allowed access to eat those foods. A marked rise in blood pressure in unrestrained marmosets was observed in response both to the sight of highly preferred foods (anticipatory period) as well as during the actual consumption of those foods (consummatory period). Excitotoxic lesions of the amygdala abolished the autonomic arousal in the anticipatory period, but spared both the behavioural arousal in the anticipatory period and the autonomic arousal in the consummatory period. Together these data serve as an important step towards understanding the role of autonomic arousal in emotion and its neural underpinnings.
Successful adaptation to changes in an animal's emotional and motivational environment depends on behavioral flexibility accompanied by changes in bodily responses, e.g., autonomic and endocrine, which support the change in behavior. Here, we identify the orbitofrontal cortex (OFC) as pivotal in the flexible regulation and coordination of behavioral and autonomic responses during adaptation. Using an appetitive Pavlovian task, we demonstrate that OFC lesions in the marmoset (i) impair an animal's ability to rapidly suppress its appetitive cardiovascular arousal upon termination of a conditioned stimulus and (ii) cause an uncoupling of the behavioral and autonomic components of the adaptive response after reversal of the reward contingencies. These findings highlight the role of the OFC in emotional regulation and are highly relevant to our understanding of disorders such as schizophrenia and autism in which uncoupling of emotional responses may contribute to the experiential distress and disadvantageous behavior associated with these disorders.behavioral inhibition ͉ emotion ͉ reversal learning T he orbitofrontal cortex (OFC) has long been implicated in behavioral f lexibility as measured by tests of discrimination reversal learning and extinction (1, 2). In reversal learning, an animal is first taught to respond to one of two visual stimuli to receive food reward, a response to the other being unrewarded. Lesions of the OFC do not affect initial acquisition of the visual discrimination, but the ability to alter responding when the association between the stimuli and reward is reversed is markedly impaired across a range of species (3-9). Similarly, animals with OFC lesions display prolonged responding during extinction when the response no longer results in the receipt of food reward (1, 10, 11). However, an alteration in behavioral output is just one component of the overall adaptive response of an animal to changes in its environment. It is important to recognize that behavioral adaptation is accompanied by alterations in the bodily state, including autonomic and endocrine activity, appropriate to the motivational and emotional context. Thus, Pavlov showed that dogs stopped salivating to a buzzer when it no longer predicted reward (12), and, had the behavioral response also been measured, it would have presumably shown that they stopped approaching the buzzer too. Indeed, if, despite inhibiting their salivation during extinction, Pavlov's dogs found themselves still approaching the buzzer, or vice versa, such incongruency between the somatic and autonomic feedback might be expected to produce emotional ambiguity, an issue that will be considered in more detail in Discussion.Currently, we have very little understanding of the neural circuitry underlying the coordination of behavioral and bodily responses in adaptive responding. Although the OFC is critical for behavioral adaptation, its role in the overall coordination of the adaptive response is unknown. Indeed, few studies have investigated the role of the O...
This paper will review two avenues of our research in marmosets that have focused on the role of the orbitofrontal cortex (OFC) in amygdala-dependent appetitive behavior. The first demonstrates the important contribution of both the OFC and the amygdala to conditioned reinforcement (CRF). The second reveals the regulatory effects of the OFC on amygdala-dependent autonomic and behavioral arousal in appetitive conditioning. The process of CRF is one way in which an environmental cue can guide emotional behavior. As a consequence of its previous relationship with reward, a cue can take on affective value and reinforce behavior. Lesion studies in marmosets are described that show that CRF is dependent upon both the amygdala and OFC. The synergistic interactions between these structures that have been shown to underlie other aspects of reward processing are then considered with respect to CRF. The results are contrasted with those that show the importance of the OFC in suppressing positive affective responses elicited by the amygdala in response to a conditioned stimulus (CS). Specifically, it will be shown that the OFC is involved in the rapid suppression of conditioned autonomic arousal upon CS withdrawal and in the co-ordination of conditioned autonomic and behavioral responses when adapting to changing reward contingencies. It will be argued that, overall, the OFC plays a critical role in the context-dependent regulation of positive affective responding governed by external cues, in keeping with a role in executive control.
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