Amygdala-hippocampal oscillatory dynamics during learning and extinction with intracranial EEG
Poster No:
605
Submission Type:
Abstract Submission
Authors:
Saurabh Sonkusare1, Yingying Zhang2, Qiong Ding3, Yashu Feng4, Alekhya Mandali5, Yijie Zhao4, Wei Liu6, Rouqi Yang6, Chencheng Zhang4, Chunyan Cao6, Bomin Sun6, Shikun Zhan6, Valerie Voon4
Institutions:
1The University of Newcastle, Australia, Newcastle, Australia, 2Fudan University, , Shanghai, China, 3The University of Cambridge, UK, Cambridge, United Kingdom, 4Fudan University, Shanghai, China, 5The University of Sheffield, Sheffield, United Kingdom, 6Ruijin Hospital, Shanghai, China
First Author:
Co-Author(s):
Introduction:
Organisms exhibit the ability to form complex associations between environmental stimuli and resulting outcomes, facilitating adaptive behaviours that are crucial for survival. Across species, these are underpinned predominantly by the amygdala and the hippocampus. Yet their precise neural dynamics and connectivity during paradigms of conditioning and extinction remains poorly characterised in humans. The amygdala is pivotal for emotional processing and plays a key role in acquiring and expressing conditioned fear. It integrates emotionally salient information and exhibits dynamic activity, including rapid habituation during both conditioning and extinction (Phelps & LeDoux, 2005; Milad et al., 2007).
Methods:
We acquired intracranial neuronal recordings from amygdala and hippocampus from a cohort of 28 patients with epilepsy undergoing stereoEEG evaluation. We localised the electrodes in the amygdala and the hippocampus (Fig 1A) Illustration of the task paradigm is shown in Fig 1B. Two different shapes (triangle and square) constituted the conditioned stimuli (CS). CS were presented for 2s and followed with an unconditioned stimulus (US) - negative (CS triangle) or neutral (CS square) valence IAPS images negative (US; contingency of 100%). The US delivery occurred upon the termination of CS (i.e., delay conditioning) and lasted for 2s. Twenty four hours after the conditioning phase, we tested the extinction phase where the CS+ were randomly presented for the same durations (2s) as in the conditioning phase but without being followed up by the negative or neutral images. We characterised task induced spectral dynamics and used permutation testing to assess condition differences. Time-frequency clusters showing condition differences were then tested for their association with behavioural emotional valence ratings of the negative and neutral images. We also conducted functional connectivity analysis with phase locking values and phase amplitude coupling.
·Figure 1. Localization of electrode contacts and task paradigm. A Amygdala shown in pink and hippocampus shown in blue. Each dot is an electrode contact. B Conditioning and extinction task paradigm.
Results:
For amygdala, condition differences in the theta (4-8 Hz) and gamma (30-45 Hz) frequency range activity were found with greater activity in the CS+ for negative US than CS+ for neutral US (Fig 2A top). During extinction phase, condition differences for amygdala were found in the same frequency bands (theta and gamma) but with opposing pattern i.e. CS+ (for negative) showed reduced activity in theta and gamma bands relative to CS+ (neutral) (Fig 2A bottom). For hippocampus conditioning phase, condition differences in the alpha (8-14 Hz) and gamma frequency range activity were found with greater activity in the CS+ for negative US than CS+ for neutral images. During extinction, hippocampus showed condition difference in theta, alpha and gamma bands with greater activity for CS+ used for pairing with negative images (Fig 2A bottom). Amygdala mean cluster differences for condition difference in the theta band was predictive of the valence ratings of negative and neutral images which were used as US, i.e greater theta activity was associated with greater negative valence (Figure 2C) (R2= .48, pFDR=.01). Connectivity analysis between amygdala and hippocampus showed robust phase synchronisation in theta frequencies with no condition differences(p>.05). Finally, cross frequency coupling analysis showed theta/alpha frequencies coupled with gamma frequencies for both amygdala and hippocampus.
·Figure 2. Task induced responses and condition differences shown in black outlines for (A) amygdala and (B) hippocampus. (C)The mean condition differences were then used to predict valence ratings
Conclusions:
These findings underscore the unique contributions of amygdala-hippocampus dynamics within a conditioning-extinction paradigm with direct human neuronal recordings. Furthermore, they provide critical insights into the neurophysiological mechanisms underlying fear learning and adaptive behaviour, offering clinical relevance for neuropsychiatric conditions such as post-traumatic stress disorder, depression, and anxiety
Emotion, Motivation and Social Neuroscience:
Emotional Learning 1
Novel Imaging Acquisition Methods:
EEG
Imaging Methods Other 2
Keywords:
ELECTROCORTICOGRAPHY
ELECTROPHYSIOLOGY
Emotions
Epilepsy
1|2Indicates the priority used for review
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Provide references using APA citation style.
Milad, M. R., Wright, C. I., Orr, S. P., Pitman, R. K., Quirk, G. J., & Rauch, S. L. (2007). Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biological psychiatry, 62(5), 446-454.