The functional profile of the human amygdala in affective processing: Insights from intracranial recordings

The amygdala is suggested to serve as a key structure in the emotional brain, implicated in diverse affective processes. Still, the bulk of existing neuroscientific investigations of the amygdala relies on conventional neuroimaging techniques such as fMRI, which are very useful but subject to limitations. These limitations are particular to their temporal resolution, but also to their spatial precision at a very fine-grained level. Here, we review studies investigating the functional profile of the human amygdala using intracranial electroencephalography (iEEG), an invasive technique with high temporal and spatial precision. We conducted a systematic literature review of 47 iEEG studies investigating the human amygdala, and we focus on two content-related domains and one process-related domain: (1) memory formation and retrieval; (2) affective processing; and (3) latency components. This review reveals the human amygdala to engage in invariant semantic encoding and recognition of specific objects and individuals, independent of context or visuospatial attributes, and to discriminate between familiar and novel stimuli. The review highlights the amygdala's role in emotion processing witnessed in differential treatment of social-affective facial cues, differential neuronal firing to relevant novel stimuli, and habituation to familiar affective stimuli. Overall, the review suggests the amygdala plays a key role in the processing of affective relevance. Finally, this review delineates effects on amygdala neuronal activity into three time latency windows (post-stimulus onset). The early window (∼ 5 0-290 msec) subsumes effects respective to exogenous stimulus-driven affective processing of faces and emotion. The intermediate window (∼ 270-470 msec) comprises effects related to explicit attention to novel task-relevant stimuli, irrespective of sensory modality. The late window (∼ 600-1400 msec) subsumes effects from tasks soliciting semantic associations and working memory during affective processing. We juxtapose these iEEG data with current clinical topics relevant to amygdala activation and propose avenues for future investigation of the amygdala using iEEG methods.