Human single-neuron activity is modulated by intracranial theta burst stimulation of the basolateral amygdala

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Detalles Bibliográficos
Publicado en:bioRxiv (Feb 15, 2025)
Autor principal: Campbell, Justin M
Otros Autores: Cowan, Rhiannon L, Wahlstrom, Krista L, Hollearn, Martina K, Jensen, Dylan, Davis, Tyler, Rahimpour, Shervin, Shofty, Ben, Arain, Amir, Rolston, John D, Hamann, Stephan, Wang, Shuo, Eisenman, Lawrence N, Swift, James, Xie, Tao, Brunner, Peter, Manns, Joseph R, Inman, Cory S, Smith, Elliot H, Willie, Jon T
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Cold Spring Harbor Laboratory Press
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022 |a 2692-8205 
024 7 |a 10.1101/2024.11.11.622161  |2 doi 
035 |a 3127415735 
045 0 |b d20250215 
100 1 |a Campbell, Justin M 
245 1 |a Human single-neuron activity is modulated by intracranial theta burst stimulation of the basolateral amygdala 
260 |b Cold Spring Harbor Laboratory Press  |c Feb 15, 2025 
513 |a Working Paper 
520 3 |a Direct electrical stimulation of the human brain has been used for numerous clinical and scientific applications. Previously, we demonstrated that intracranial theta burst stimulation (TBS) of the basolateral amygdala (BLA) can enhance declarative memory, likely by modulating hippocampal-dependent memory consolidation. At present, however, little is known about how intracranial stimulation affects activity at the microscale. In this study, we recorded intracranial EEG data from a cohort of patients with medically refractory epilepsy as they completed a visual recognition memory task. During the memory task, brief trains of TBS were delivered to the BLA. Using simultaneous microelectrode recordings, we isolated neurons in the hippocampus, amygdala, orbitofrontal cortex, and anterior cingulate cortex and tested whether stimulation enhanced or suppressed firing rates. Additionally, we characterized the properties of modulated neurons, patterns of firing rate coactivity, and the extent to which modulation affected memory task performance. We observed a subset of neurons (~30%) whose firing rate was modulated by TBS, exhibiting highly heterogeneous responses with respect to onset latency, duration, and direction of effect. Notably, location and baseline activity predicted which neurons were most susceptible to modulation, although the impact of this neuronal modulation on memory remains unclear. These findings advance our limited understanding of how focal electrical fields influence neuronal firing at the single-cell level and motivate future neuromodulatory therapies that aim to recapitulate specific patterns of activity implicated in cognition and memory.Competing Interest StatementThe authors have declared no competing interest.Footnotes* The manuscript has been restructured as a full-length research article, with numerous updates to the text and figures (style and substance). Additionally, we have implemented a new population-level analysis of neuronal coactivity, shown in Figure 3F and Supplemental Figure 3. 
653 |a Emotions 
653 |a Memory 
653 |a Autonomic nervous system 
653 |a Amygdala 
653 |a Neurons 
653 |a Cognition 
653 |a Electrophysiological recording 
653 |a Hippocampal plasticity 
653 |a Temporal lobe 
653 |a Mental task performance 
653 |a Visual pathways 
653 |a Neuromodulation 
653 |a Firing rate 
653 |a Long-term potentiation 
653 |a Synaptic plasticity 
653 |a Latency 
653 |a Visual stimuli 
653 |a Theta rhythms 
653 |a Electrical stimuli 
700 1 |a Cowan, Rhiannon L 
700 1 |a Wahlstrom, Krista L 
700 1 |a Hollearn, Martina K 
700 1 |a Jensen, Dylan 
700 1 |a Davis, Tyler 
700 1 |a Rahimpour, Shervin 
700 1 |a Shofty, Ben 
700 1 |a Arain, Amir 
700 1 |a Rolston, John D 
700 1 |a Hamann, Stephan 
700 1 |a Wang, Shuo 
700 1 |a Eisenman, Lawrence N 
700 1 |a Swift, James 
700 1 |a Xie, Tao 
700 1 |a Brunner, Peter 
700 1 |a Manns, Joseph R 
700 1 |a Inman, Cory S 
700 1 |a Smith, Elliot H 
700 1 |a Willie, Jon T 
773 0 |t bioRxiv  |g (Feb 15, 2025) 
786 0 |d ProQuest  |t Biological Science Database 
856 4 1 |3 Citation/Abstract  |u https://www.proquest.com/docview/3127415735/abstract/embedded/7BTGNMKEMPT1V9Z2?source=fedsrch 
856 4 0 |3 Full Text - PDF  |u https://www.proquest.com/docview/3127415735/fulltextPDF/embedded/7BTGNMKEMPT1V9Z2?source=fedsrch 
856 4 0 |3 Full text outside of ProQuest  |u https://www.biorxiv.org/content/10.1101/2024.11.11.622161v2