Cross-regional coordination of activity in the human brain during autobiographical self- referential processing

• 成果类型: Article
• 署名作者: Stieger, James R.; Pinheiro-Chagas, Pedro; Fang, Ying; Li, Jian; Lusk, Zoe; Perry, Claire M.; Girn, Manesh; Contreras, Diego; Chen, Qi; Huguenard, John R.; Spreng, R. Nathan; Edlow, Brian L.; Wagner, Anthony D.; Buch, Vivek; Parvizi, Josef
• 署名单位: Stanford University; Stanford University; South China Normal University; Harvard University; Harvard University Medical Affiliates; Massachusetts General Hospital; McGill University; University of Pennsylvania; Stanford University; Stanford University
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-14162
• DOI: 10.1073/pnas.2316021121
• 发表日期: 2024-08-06
• 关键词: medial prefrontal cortex; episodic memory; anterior nucleus; functional neuroanatomy; orbitofrontal cortex; decision-making; parietal cortex; network; theta; thalamus

摘要

For the human brain to operate, populations of neurons across anatomical structures must coordinate their activitywithin milliseconds. To date, our understanding of such interactions has remained limited. We recorded directly from the hippocampus (HPC), posteromedial cortex (PMC), ventromedial/orbital prefrontal cortex (OFC), and the anterior nuclei of the thalamus (ANT) during two experiments of autobiographical memory processing that are known from decades of neuroimaging work to coactivate these regions. In 31 patients implanted with intracranial electrodes, we found that the presentation of memory retrieval cues elicited a significant increase of low frequency (LF < 6 Hz) activity followed by cross- regional phase coherence of this LF activity before select populations of neurons within each of the four regions increased high- frequency (HF > 70 Hz) activity. The power of HF activity was modulated by memory content, and its onset followed a specific temporal order ofANT -> HPC/PMC -> OFC. Further, we probed cross- regional causal effective interactions with repeated electrical pulses and found that HPC stimulations cause the greatest increase in LF-phase coherence across all regions, whereas the stimulation of any region caused the greatest LF-phase coherence between that particular region and ANT. These observations support the role of the ANT in gating, and the HPC in synchronizing, the activity of cortical midline structures when humans retrieve self- relevant memories of their past. Our findings offer a fresh perspective, with high temporal fidelity, about the dynamic signaling and underlying causal connections among distant regions when the brain is actively involved in retrieving self- referential memories from the past.