Intracranial-EEG evidence for medial temporal pole driving amygdala activity induced by multi-modal emotional stimuli

Abstract

The temporal pole (TP) is an associative cortical region required for complex cognitive functions such as social and emotional cognition. However, functional mapping of the TP with functional magnetic resonance imaging is technically challenging and thus understanding of its interaction with other key emotional circuitry, such as the amygdala, remain elusive. We exploited the unique advantages of stereo-electroencephalography (SEEG) to assess the responses of the TP and the amygdala during the perception of emotionally salient stimuli of pictures, music and movies. These stimuli consistently elicited high gamma responses (70-140 Hz) in both the TP and the amygdala, accompanied by functional connectivity in the low frequency range (2-12 Hz). Computational analyses suggested the TP driving this effect in the theta-alpha frequency range and which was modulated by the emotional salience of the stimuli. Of note, cross-frequency analysis indicated the phase of theta-alpha oscillations in the TP modulated the amplitude of high gamma activity in the amygdala. These results were reproducible with three types of stimuli including naturalistic stimuli suggesting a hierarchical influence of the TP over the amygdala in non-threatening stimuli.

Brain hemodynamic response in Examiner–Examinee dyads during spatial short-term memory task: an fNIRS study

“…Conversely, when Examinees produced spatial movements not matching the given sequences, such as higher load conditions producing more errors in general, their brain activity decreased, and Examiners’ brain activity decreased as well. Independently from the exact cognitive processes put in motion, these data are in line with recent studies on brain synchronization (Cui et al 2012 ; Dommer et al 2012 ; Jiang et al 2012 ; Liu et al 2012 , 2015 , 2016 ; Baker et al 2016 ; Nguyen et al 2020 ), showing larger cortical hemodynamic responses during cooperative or conjoint activities, and on functional and neural similarities between action and perception (Meltzoff and Decety 2003 ; Kokal et al 2009 ). In the field of neuropsychological testing, these results are highly relevant, as they seem to suggest a complex interaction between the Examiner and the Examinee during clinical assessment.…”

“…In line with previous neuroimaging studies (Bor et al 2006 ; Toepper et al 2010 ), we expected that CBT execution would induce PFC activity and that this activity would increase as a function of the workload in the Examinees. Moreover, in line with previous findings on neural synchrony (Cui et al 2012 ; Dommer et al 2012 ; Jiang et al 2012 ; Liu et al 2015 , 2016 ; Baker et al 2016 ; Nguyen et al 2020 ), and on shared common codes between action and perception (Meltzoff and Decety 2003 ; Kokal et al 2009 ) we also speculated that the Examinees’ and Examiners’ brain activation in the dyads would parallel each other during the task.…”

“…For instance, Liu et al ( 2016 ) showed increased inter-brain neural synchronization in PFC during a naturally occurring cooperative task involving face-to-face communication. Inter-brain synchrony was observed when participants performed the task together but not during an individual condition (Cui et al 2012 ; Dommer et al 2012 ; Jiang et al 2012 ; Liu et al 2015 ; Baker et al 2016 ; Nguyen et al 2020 ). In the real CBT administration, mimicking the sequences produced by another person can be considered as a form of imitation of movements directed toward spatial positions, and some findings support the hypothesis that action perception shares the same mechanisms as action performance (Meltzoff and Decety 2003 ; Kokal et al 2009 ).…”

Intracranial EEG spectral feature analysis and focal brain stimulation reveal affective specialization within dorsal anterior cingulate cortex

“…Conventional approaches of analyzing EEG neural data have relied on restricting analysis to a predefined canonical frequency band (i.e., theta, alpha, etc. ); neural activity gets defined as power in an arbitrarily defined oscillatory bands, which are kept the same for analyses over all brain regions for scalp EEG 29,30 and intracranial EEG 37,38 . However, recent findings cast doubt on this approach showing that the dominant frequency of an oscillation, or neural feature, can vary along an anatomical dimension 39 .…”

Right Hemisphere Dominance for Unconscious Emotionally Salient Stimuli

“…An influential model on emotional processing has postulated the existence of multiple pathways, involving both cortical and subcortical structures [34], that convey threat-related information to this subcortical structure. More precisely, the fine-grained and conscious evaluation of potentially dangerous stimuli has been proposed to rely on a cortical "high road" pathway, in which relevant visual information, originating from lower order visual regions, such as the thalamic lateral geniculate nucleus and the striate cortex, traverse the ventral temporal cortices to reach the amygdala [35] and, at a later stage, the prefrontal cortex for higher-level emotional and cognitive evaluation [36,37]. On the contrary, both human and non-human animals have evolved a direct pathway to the amygdala, bypassing the primary sensory cortices, which allows rapid and automatic responses to danger.…”