Dataset Information

Distinct Processing of Aversive Experience in Amygdala Subregions.

ABSTRACT:

Background

The amygdala is an anatomically complex medial temporal brain structure whose subregions are considered to serve distinct functions. However, their precise role in mediating human aversive experience remains ill understood.

Methods

We used functional magnetic resonance imaging in 39 healthy volunteers with varying levels of trait anxiety to assess distinct contributions of the basolateral amygdala (BLA) and centromedial amygdala to anticipation and experience of aversive events. Additionally, we examined the relationship between any identified functional subspecialization and measures of subjective reported aversion and trait anxiety.

Results

Our results show that the centromedial amygdala is responsive to aversive outcomes but insensitive to predictive aversive cues. In contrast, the BLA encodes an aversive prediction error that quantifies whether cues and outcomes are worse than expected. A neural representation within the BLA for distinct threat levels was mirrored in self-reported subjective anxiety across individuals. Furthermore, high trait-anxious individuals were characterized by indiscriminately heightened BLA activity in response to aversive cues, regardless of actual threat level.

Conclusions

Our results demonstrate that amygdala subregions are distinctly engaged in processing of aversive experience, with elevated and undifferentiated BLA responses to threat emerging as a potential neurobiological mediator of vulnerability to anxiety disorders.

SUBMITTER: Michely J

PROVIDER: S-EPMC7059109 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Three subregions of the amygdala receive monosynaptic projections from the olfactory bulb, making them part of the primary olfactory cortex. These primary olfactory areas are located at the anterior-medial aspect of the amygdala and include the medial amygdala (MeA), cortical amygdala (CoA), and the periamygdaloid complex (PAC). The vast majority of research on the amygdala has focused on the larger basolateral and basomedial subregions, which are known to be involved in implicit learning, threat responses, and emotion. Fewer studies have focused on the MeA, CoA, and PAC, with most conducted in rodents. Therefore, our understanding of the functions of these amygdala subregions is limited, particularly in humans. Here, we first conducted a review of existing literature on the MeA, CoA, and PAC. We then used resting-state fMRI and unbiased k-means clustering techniques to show that the anatomical boundaries of human MeA, CoA, and PAC accurately parcellate based on their whole-brain resting connectivity patterns alone, suggesting that their functional networks are distinct, relative both to each other and to the amygdala subregions that do not receive input from the olfactory bulb. Finally, considering that distinct functional networks are suggestive of distinct functions, we examined the whole-brain resting network of each subregion and speculated on potential roles that each region may play in olfactory processing. Based on these analyses, we speculate that the MeA could potentially be involved in the generation of rapid motor responses to olfactory stimuli (including fight/flight), particularly in approach/avoid contexts. The CoA could potentially be involved in olfactory-related reward processing, including learning and memory of approach/avoid responses. The PAC could potentially be involved in the multisensory integration of olfactory information with other sensory systems. These speculations can be used to form the basis of future studies aimed at clarifying the olfactory functions of these under-studied primary olfactory areas.