Scientific Understanding of Consciousness
Orbitofrontal–Amygdala Circuit and Social–Emotional Behavior
Neuroscience and Biobehavioral Reviews 30 (2006) 97–117
The orbitofrontal–amygdala circuit and self-regulation of social–emotional behavior in autism
Jocelyne Bachevalier, Katherine A. Loveland
Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA
Department of Psychiatry and Behavioral Sciences, University of Texas Medical School, University of Texas Health Science Center, Houston, TX, USA
The anatomical organization of the orbitofrontal–amygdala circuit
Social cognition is realized through a complex neural network of interconnected structures, which includes the ventromedial portion of the prefrontal cortex, the amygdala within the temporal lobe, and their interconnections with the hypothalamus and brain stem. Anatomical studies have further demonstrated that two major subsystems appear to feed into this limbic system. One is a system centered around the hippocampus, which comprises the posterior cingulate cortex and parahippocampal gyri, anterior thalamic nuclei, and the parietal and dorsolateral prefrontal cortex. This dorsal circuit appears to monitor the online-processing of sensory events and current actions in the service of the visuospatial domain and memory. The second is a ventral circuit centered around the amygdala, which includes the anterior cingulate and orbital frontal cortex and the mediodorsal nucleus of the thalamus. This ventral circuit has been implicated in the monitoring of emotional states and social cognition as well as in the self-regulation of behavior through knowledge of emotional responses and intentions of others.
The amygdala, located in the anterior portion of the medial temporal lobe, comprises a set of thirteen interconnected nuclei with different connectional features. Its cytological components and interconnections have been extensively studied in monkeys and share strong similarity with those of humans. Briefly, the lateral nucleus receives an enormous array of highly processed sensory information, including visual information from faces and facial expressions, gaze direction, body postures and movements, as well as auditory information from specific vocal sounds and intonations. Reciprocally, via the basal nucleus, it provides a route by which affective states can modulate the cortical processing of sensory stimuli. Interestingly, because these feedback projections from the amygdala to the cortical sensory areas are widespread, reaching not only the association cortical areas but also the primary sensory cortical areas, emotional states could influence sensory inputs at very early stages in their processing, by weighting the emotional significance of sensory information. The central nucleus provides a relay to the brainstem and hypothalamus through which the amygdala is thought to influence the autonomic and endocrine manifestations of emotion, respectively. Via this pathway, sensory stimuli could influence and activate emotional reactions. The basal and accessory basal nuclei project substantially to the ventral striatum, thereby offering a way by which affective states could provide access to subcortical elements of the motor system and so affect actions, including the modulation of facial and vocal expressions, body postures and movements. In addition, the amygdala significantly interacts with the hippocampal formation, and can thus act upon and modulate stored information in cortical areas (e.g. past experience with an individual).
The orbital region of the prefrontal cortex is a mesiocortical area that occupies the ventral surface of the frontal lobe. Comparative anatomical studies have indicated that the orbitofrontal cortex shares great similarities among primates, including humans, and that it can be subdivided into distinct cortical areas. Like the amygdala, it receives highly-processed information from all sensorymodalities (visual, somatosensory, visceral, olfactory, and gustatory) and, based on the pattern of its connectivity, it has been divided into medial and lateral networks. The medial network of the orbital frontal cortex, e.g. area 14 in monkey, has strong connections with the hippocampus and associated areas of the cingulate, retrosplenial, and entorhinal cortices. The lateral network has been further subdivided into a caudal sector, e.g. areas 12 and 13, that is mainly interconnected with the amygdala, midline thalamus, and temporal pole, and a rostral sector, e.g. areas 12 and 11, that has more pronounced connections with the insula, mediodorsal nucleus of the thalamus, inferior parietal lobule and dorsolateral prefrontal cortex. Interestingly, the orbital frontal cortex differs in many ways from the most dorsolateral prefrontal region. For example, unlike the dorsolateral prefrontal area, which receives projections primarily from the mediodorsal nucleus of the thalamus, the orbital frontal area receives projections primarily from midline and intralaminar nuclei. In addition, the orbital frontal cortex receives robust projections from both the amygdala and the temporopolar area, whereas the rest of the prefrontal cortex appears to have few, if any, links with the amygdala and temporal pole. Thus, unlike the dorsolateral aspect of the prefrontal cortex, the orbital frontal area receives information about all aspects of the external and internal environment, from thalamic nuclei involved in associative aspects of memory, and from the amygdala and temporal pole that are thought to regulate emotional states. Thus, the connections between the amygdala and orbital frontal cortex may permit the modulation and self-regulation of emotional behavior in relation to rapid changes in a social situation or context (e.g. dominance relationships, situational features). Finally, the orbital frontal cortex also sends inputs to brain regions, such as the preoptic region of the lateral hypothalamus, that are critical for hormonal modulation of emotions, and to motor centers, such as the head of the caudate and the ventral tegmental area, that are critical for motor control of emotional behaviors.
In sum, the anatomical organization and reciprocal relationship between the amygdala and orbitofrontal cortex implies that these brain regions may share a close functional relationship within a system essential for the maintenance of intra-specific social bonding and the self-regulation of emotional states. Converging evidence from rodents, humans, and non-human primates indicates that the interconnections between the basolateral complex of the amygdala and the orbital frontal cortex are crucial to the formation and use of expectancies for reinforcers in the guidance of goal-directed behavior. Yet, the mechanisms by which these neural structures participate in social cognition are still poorly understood and it is unknown whether the specific mechanisms related to each structure can be distinguished or whether these neural structures function as a unitary ‘system’. Nevertheless, there exists some evidence to suggest that each component of this neural network may contribute differently to the control of social cognition.
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