Sequence of information processing for emotions through pathways linking temporal and insular cortices with the amygdala

The amygdala has a pivotal role in deciphering the emotional significance of sensory stimuli enabling emotional memory formation. We have previously shown that prefrontal cortices in rhesus monkeys project to the amygdala mainly from their deep layers, suggesting feedback communication. If sensory areas convey signals pertinent to the state of the environment, they should issue feedforward projections to the amygdala, arising mainly from the upper layers, consistent with the flow of information from earlier- to later-processing sensory cortices. Here we addressed this hypothesis in cases with injection of tracers in sites of the amygdala known to have robust connections with prefrontal cortices and mapped connections in insular and temporal cortices associated with sensory processing and memory. The medial temporal pole, the entorhinal and perirhinal areas, and the agranular and dysgranular insula had the densest connections with the amygdala, and the lateral temporal pole, the parahippocampal region, and the granular insula had sparser connections. Most areas projected to the amygdala predominantly from the upper layers, suggesting feedforward communication, and received reciprocal amygdalar innervation primarily in their superficial layers, suggesting feedback communication. In contrast, the entorhinal cortex issued projections to the amygdala from its deep layers, suggesting feedback communication, and received reciprocal amygdalar projections most densely in layers II-III, which project to the hippocampus. These findings may help explain how the amygdala can attach emotional value to environmental stimuli, participate in the sequence of information processing of emotions, and modulate the formation of emotional memories.