Integrative roles of human amygdala subdivisions: Insight from direct intracerebral stimulations via stereotactic EEG

• Published in: Human brain mapping 2023-06, Vol.44 (9), p.3610-3623
• Main Authors: Zhang, Huaqiang, Wang, Di, Wei, Penghu, Fan, Xiaotong, Yang, Yanfeng, An, Yang, Dai, Yang, Feng, Tao, Shan, Yongzhi, Ren, Liankun, Zhao, Guoguang
• Format: Article
• Language: English
• Subjects: Amygdala; Amygdala - diagnostic imaging; Amygdala - physiology; Autonomic nervous system; Circuits; Drug resistance; Electric Stimulation; Electrical properties; electrical stimulation; Electrical stimuli; Electrodes; Electroencephalography; Emotional factors; Emotions; Epilepsy; Evoked Potentials - physiology; function; Hallucinations; human amygdala; Humans; Mental disorders; Neural networks; Patients; Roles; SEEG; Sensory integration; Sensory stimulation; Signs and symptoms; Software; Statistical analysis; Stereotaxic Techniques; Subdivisions; subnuclei; Substrates; Vestibular system
• ISSN: 1065-9471; 1097-0193
• DOI: 10.1002/hbm.26300

Substantial studies of human amygdala function have revealed its importance in processing emotional experience, autonomic regulation, and sensory information; however, the neural substrates and circuitry subserving functions have not been directly mapped at the level of the subnuclei in humans. We provide a useful overview of amygdala functional characterization by using direct electrical stimulation to various amygdala regions in 48 patients with drug‐resistant epilepsy undergoing stereoelectroencephalography recordings. This stimulation extends beyond the anticipated emotional, neurovegetative, olfactory, and somatosensory responses to include visual, auditory, and vestibular sensations, which may be explained by the functional connectivity with cortical and subcortical regions due to evoked amygdala‐cortical potentials. Among the physiological symptom categories for each subnucleus, the most frequently evoked neurovegetative symptoms were distributed in almost every subnucleus. Laterobasal subnuclei are mainly associated with emotional responses, somatosensory responses, and vestibular sensations. Superficial subnuclei are mainly associated with emotional responses and olfactory and visual hallucinations. Our findings contribute to a better understanding of the functional architecture of the human amygdala at the subnuclei level and as a mechanistic basis for the clinical practice of amygdala stimulation in treating patients with neuropsychiatric disorders.