Temporal dynamics of amygdala response to emotion- and action-relevance

Abstract

it has been proposed that the human amygdala may not only encode the emotional value of sensory events, but more generally mediate the appraisal of their relevance for the individual's goals, including relevance for action or task-based needs. However, emotional and non-emotional/action-relevance might drive amygdala activity through distinct neural signals, and the relative timing of both kinds of responses remains undetermined. Here, we recorded intracranial event-related potentials from nine amygdalae of patients undergoing epilepsy surgery, while they performed variants of a Go/NoGo task with faces and abstract shapes, where emotion-and action-relevance were orthogonally manipulated. Our results revealed early amygdala responses to emotion facial expressions starting ~ 130 ms after stimulus-onset. Importantly, the amygdala responded to action-relevance not only with face stimuli but also with abstract shapes (squares), and these relevance effects consistently occurred in later time-windows (starting ~ 220 ms) for both faces and squares. A similar dissociation was observed in gamma activity. Furthermore, whereas emotional responses habituated over time, the actionrelevance effect increased during the course of the experiment, suggesting progressive learning based on the task needs. Our results support the hypothesis that the human amygdala mediates a broader relevance appraisal function, with the processing of emotion-relevance preceding temporally that of action-relevance. The amygdala is a crucial component of brain circuits allowing swift reaction to threatening stimuli, an ability critical for adaptive behavior and survival 1,2. Fast and efficient discrimination of potentially harmful events is a hallmark of the fear response, associated with a well-established sensitivity of the amygdala to threat information, and extensive connectivity with multiple other brain regions that act to facilitate attention, enhance memory, and promote actions 3. It has recently been questioned, however, whether the amygdala is dedicated to fear processing 1 or whether instead it may serve a broader function for the appraisal of behaviorally relevant events (see 4 for a review). There is abundant evidence that the human amygdala responds to other emotionally significant stimuli beyond threat 5 , including positive or reward information 6,7 , but also novelty 8 and non-emotional salient stimuli with personal impact or goal-related significance 9,10. This diversity of response patterns has led to recent theoretical accounts proposing that the amygdala may actually encode the "relevance" of events, which is determined by the goals,

Snakes vs. Guns: A Systematic Review of Comparisons Between Phylogenetic and Ontogenetic Threats

“…Two other brain imaging studies (Cao et al 2014;Fang et al,2016) further supports the notion of different brain mechanisms for these threats but the patterns of higher and lower amygdala activation in response to threats depending on the presence or absence of human context depicts amygdala as a more flexible module for appraisal of relevance (Guex et al, 2020) than a rigid module of fear. Once again, looking at amygdala as the relevance detector (Sanders, et al, 2003) is a better explanation of the findings than fear module theory.…”

Snakes vs. Guns: a Systematic Review of Comparisons Between Phylogenetic and Ontogenetic Threats

“…Two other brain imaging studies (Cao et al 2014;Fang et al,2016) further supports the notion of different brain mechanisms for these threats but the patterns of higher and lower amygdala activation in response to threats depending on the presence or absence of human context depicts the amygdala as a more flexible module for appraisal of relevance (Guex et al, 2020) than a rigid module of fear. Once again, looking at the amygdala as the relevance detector (Sanders, et al, 2003) is a better explanation of the findings than fear module theory.…”

Emotional context sculpts action goal representations in the lateral frontal pole

“…Such abstract representations may provide important conceptual knowledge about when (and how) to respond to emotional events (Saez et al 2015). Relatedly, amygdala intracranial event related potentials (iERPs) during an AGNG task represent the interaction of emotional valence (negative vs. neutral) and task rule (Go vs. No-Go) (Guex et al 2020). Together, these results demonstrate a broader, more goal-oriented and contextually sensitive role for amygdala neurons than its more commonly emphasized emotional valence and arousal encoding functions (Pignatelli and Beyeler 2019).…”