Amygdala beta bursts modulate hippocampal neuronal dynamics during human emotional processing

The amygdala and hippocampus are key structures in emotional processing, yet the transient neural dynamics coordinating their interaction remain poorly understood. We simultaneously recorded single-neuron activity and local field potentials from these regions in epilepsy patients performing an emotional image-rating task. Neurons in both regions exhibited firing rate changes predictive of subjective emotional valence.

While conventional spectral analysis revealed no valence-specific patterns, beta bursts (13-30 Hz)–transient, high-power events–were selectively modified by task features. In both regions, beta bursts were associated with increased gamma amplitude and enhanced phase coherence, with beta-gamma phase-amplitude coupling capturing emotion-related dynamics. Critically, amygdala beta bursts were associated with valence-dependent, bidirectional modulation of hippocampal interneuron firing – decreased during very unpleasant/highest arousal processing and increased during high-arousal very pleasant processing – while putative pyramidal-cell firing did not change significantly.

Hippocampal bursts showed no reciprocal influence. These findings suggest that beta bursts may represent a temporally precise neural correlate of emotional appraisal and a potential target for neuromodulation in mood disorders. We thank the members of the Yale Comprehensive Epilepsy Center for their excellent patient care, the patients who participated in this study.

This study was supported by grants from the National Institutes of Health (R01MH138291 ECD); The Hypothesis Fund Seed Grant (ECD), Center for Brain and Mind Health (ECD, AK, IHR, AS), VA National Center for PTSD and Wellcome Trust Grant: 310142/Z/24/Z (ECD, AK, IHR and JK). These authors contributed equally: Yajun Zhou, Yuqing Huang. Department of Neurosurgery, Yale University, New Haven, CT, USA Yajun Zhou, Yuqing Huang, Giana F.

Pittaro, Behzad Zareian, Ayman Aljishi, Alondra P. Toro, Zion Zibly, Sami Obaid & Eyiyemisi C. Damisah Department of Neurology, Yale University, New Haven, CT, USA Department of Psychiatry, Yale University, New Haven, CT, USA Ilan Harpaz-Rotem, Alfred Kaye, John Krystal, Xiaosi Gu & Christopher Pittenger Wu Tsai Institute, Yale University, New Haven, CT, USA Ilan Harpaz-Rotem, Alfred Kaye, John Krystal, Christopher Pittenger & Eyiyemisi C.

Damisah Clinical Neurosciences Division, VA National Center for PTSD, West Haven, CT, USA Department of Neuroscience, Yale University, New Haven, CT, USA Department of Psychology, Yale University, New Haven, CT, USA Center for Brain and Mind Health, Yale University, New Haven, CT, USA Christopher Pittenger & Eyiyemisi C. Damisah The authors declare no competing interests. Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.