Abstract
In a complex environment that contains both opportunities and threats, it is important for an organism to flexibly direct attention based on current events and prior plans. The amygdala, the hub of the brain's emotional system, is involved in forming and signaling affective associations between stimuli and their consequences. The inhibitory thalamic reticular nucleus (TRN) is a hub of the attentional system that gates thalamo-cortical signaling. In the primate brain, a recently discovered pathway from the amygdala sends robust projections to TRN. Here we used computational modeling to demonstrate how the amygdala-TRN pathway, embedded in a wider neural circuit, can mediate selective attention guided by emotions. Our Emotional Gatekeeper model demonstrates how this circuit enables focused top-down, and flexible bottom-up, allocation of attention. The model suggests that the amygdala-TRN projection can serve as a unique mechanism for emotion-guided selection of signals sent to cortex for further processing. This inhibitory selection mechanism can mediate a powerful affective ‘framing’ effect that may lead to biased decision-making in highly charged emotional situations. The model also supports the idea that the amygdala can serve as a relevance detection system. Further, the model demonstrates how abnormal top-down drive and dysregulated local inhibition in the amygdala and in the cortex can contribute to the attentional symptoms that accompany several neuropsychiatric disorders.
Highlights
To survive in a dynamic and information-rich environment, individuals must flexibly allocate attention to emotionally salient stimuli
We studied the performance of the Emotional Gatekeeper (EmGate) model for two emotional attention paradigms: a Pavlovian conditioning experiment and an ‘attentional rubbernecking’ experiment
The EmGate model demonstrates four computational processes mediated by the circuitry linking amygdala, thalamic reticular nucleus (TRN) and cortex: (1) bottom-up shifting of both attention and behavioral plan in response to the affective salience of the presented stimulus; (2) top-down focusing of attention neurons allows basal amygdala (BA) (C) to restrict sensory attention to the stimulus that was previously associated with an aversive stimulus: CS3
Summary
To survive in a dynamic and information-rich environment, individuals must flexibly allocate attention to emotionally salient stimuli. The amygdala has been viewed as central to positive (appetitive) and negative (aversive) learning and response [12,13], as well as having a key role in motivation, memory and cognitive-emotional interactions [14,15]. Pavlovian fear conditioning studies in rodents suggest involvement of BLA as a whole in appetitive learning [18,19,20,21,22,23], based on neuronal responses to the positive and negative value of stimuli [24]. In the primate amygdala neuronal responses correlate with spatial attention to positive and negative stimuli [25]
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