Integrative roles of human amygdala subdivisions: Insight from direct intracerebral stimulations via stereotactic EEG
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 p...
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| Veröffentlicht in: | Human brain mapping 2023-06, Vol.44 (9), p.3610-3623 |
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| creator | Zhang, Huaqiang Wang, Di Wei, Penghu Fan, Xiaotong Yang, Yanfeng An, Yang Dai, Yang Feng, Tao Shan, Yongzhi Ren, Liankun Zhao, Guoguang |
| description | 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. |
| doi_str_mv | 10.1002/hbm.26300 |
| format | Article |
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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.</description><identifier>ISSN: 1065-9471</identifier><identifier>EISSN: 1097-0193</identifier><identifier>DOI: 10.1002/hbm.26300</identifier><identifier>PMID: 37073861</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>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</subject><ispartof>Human brain mapping, 2023-06, Vol.44 (9), p.3610-3623</ispartof><rights>2023 The Authors. published by Wiley Periodicals LLC.</rights><rights>2023 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). 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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.</description><subject>Amygdala</subject><subject>Amygdala - diagnostic imaging</subject><subject>Amygdala - physiology</subject><subject>Autonomic nervous system</subject><subject>Circuits</subject><subject>Drug resistance</subject><subject>Electric Stimulation</subject><subject>Electrical properties</subject><subject>electrical stimulation</subject><subject>Electrical stimuli</subject><subject>Electrodes</subject><subject>Electroencephalography</subject><subject>Emotional factors</subject><subject>Emotions</subject><subject>Epilepsy</subject><subject>Evoked Potentials - physiology</subject><subject>function</subject><subject>Hallucinations</subject><subject>human amygdala</subject><subject>Humans</subject><subject>Mental disorders</subject><subject>Neural networks</subject><subject>Patients</subject><subject>Roles</subject><subject>SEEG</subject><subject>Sensory integration</subject><subject>Sensory stimulation</subject><subject>Signs and symptoms</subject><subject>Software</subject><subject>Statistical analysis</subject><subject>Stereotaxic Techniques</subject><subject>Subdivisions</subject><subject>subnuclei</subject><subject>Substrates</subject><subject>Vestibular system</subject><issn>1065-9471</issn><issn>1097-0193</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kV1rFDEUhoNYbK1e-Ack4E29mDZfk8x4I1rWdqHijV6HM9lkNyUzqUlmy_57s24tVvDqHDgPD-_hRegNJeeUEHaxGcZzJjkhz9AJJb1qCO358_0u26YXih6jlznfEkJpS-gLdMwVUbyT9ATNy6nYdYLitxanGGzG0eHNPMKEYdytVxAA53lY-a3PPk75A15O2a83BbsUR7zyyZqC_VQSGJvskCDgXPw4h-qsPN76Kij1FAuY4g1eLK5eoSMHIdvXD_MU_fiy-H553dx8u1pefrppjBCCNIOUjCtZX7KdhJb11BmgQljhWnBSABddX3fDFBvk0KkOXAdGudZJopTkp-jjwXs3D6NdGbuPGfRd8iOknY7g9dPL5Dd6HbeaEka46ttqOHswpPhztrno0WdjQ4DJxjlr1hHOWSeoqOi7f9DbOKep_lcpqpikbbcXvj9QJsWck3WPaSjR-zZ1bVP_brOyb_-O_0j-qa8CFwfg3ge7-79JX3_-elD-AuXlquw</recordid><startdate>20230615</startdate><enddate>20230615</enddate><creator>Zhang, Huaqiang</creator><creator>Wang, Di</creator><creator>Wei, Penghu</creator><creator>Fan, Xiaotong</creator><creator>Yang, Yanfeng</creator><creator>An, Yang</creator><creator>Dai, Yang</creator><creator>Feng, Tao</creator><creator>Shan, Yongzhi</creator><creator>Ren, Liankun</creator><creator>Zhao, Guoguang</creator><general>John Wiley & Sons, Inc</general><scope>24P</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-7202-2474</orcidid><orcidid>https://orcid.org/0000-0002-1780-158X</orcidid><orcidid>https://orcid.org/0000-0002-7569-5252</orcidid><orcidid>https://orcid.org/0000-0001-5147-3068</orcidid></search><sort><creationdate>20230615</creationdate><title>Integrative roles of human amygdala subdivisions: Insight from direct intracerebral stimulations via stereotactic EEG</title><author>Zhang, Huaqiang ; 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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.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>37073861</pmid><doi>10.1002/hbm.26300</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-7202-2474</orcidid><orcidid>https://orcid.org/0000-0002-1780-158X</orcidid><orcidid>https://orcid.org/0000-0002-7569-5252</orcidid><orcidid>https://orcid.org/0000-0001-5147-3068</orcidid><oa>free_for_read</oa></addata></record> |
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| 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 |
| title | Integrative roles of human amygdala subdivisions: Insight from direct intracerebral stimulations via stereotactic EEG |
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