Infrared neural stimulation in human cerebral cortex

Li Pan; An Ping; Kenneth E Schriver; Anna Wang Roe; Junming Zhu; Kedi Xu

doi:10.1016/j.brs.2023.01.1678

Infrared neural stimulation in human cerebral cortex

Brain Stimul. 2023 Mar-Apr;16(2):418-430. doi: 10.1016/j.brs.2023.01.1678. Epub 2023 Jan 31.

Authors

Li Pan¹, An Ping², Kenneth E Schriver³, Anna Wang Roe⁴, Junming Zhu⁵, Kedi Xu⁶

Affiliations

¹ Qiushi Academy for Advanced Studies (QAAS), Zhejiang University, Hangzhou, China; Key Laboratory of Biomedical Engineering of Education Ministry, Department of Biomedical Engineering, Zhejiang Provincial Key Laboratory of Cardio-Cerebral Vascular Detection Technology and Medicinal Effectiveness Appraisal, Zhejiang University, Hangzhou, China. Electronic address: 3130103051@zju.edu.cn.
² Department of Neurosurgery, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, China. Electronic address: pingan@zju.edu.cn.
³ Interdisciplinary Institute of Neuroscience and Technology (ZIINT), School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou, China. Electronic address: kenschriver@zju.edu.cn.
⁴ Department of Neurosurgery, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, China; Interdisciplinary Institute of Neuroscience and Technology (ZIINT), School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou, China; Key Laboratory of Biomedical Engineering of Education Ministry, Department of Biomedical Engineering, Zhejiang Provincial Key Laboratory of Cardio-Cerebral Vascular Detection Technology and Medicinal Effectiveness Appraisal, Zhejiang University, Hangzhou, China; MOE Frontier Science Center for Brain Science and Brain-machine Integration, Zhejiang University, Hangzhou, China. Electronic address: annawang@zju.edu.cn.
⁵ Department of Neurosurgery, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, China; MOE Frontier Science Center for Brain Science and Brain-machine Integration, Zhejiang University, Hangzhou, China. Electronic address: dr.zhujunming@zju.edu.cn.
⁶ Qiushi Academy for Advanced Studies (QAAS), Zhejiang University, Hangzhou, China; Key Laboratory of Biomedical Engineering of Education Ministry, Department of Biomedical Engineering, Zhejiang Provincial Key Laboratory of Cardio-Cerebral Vascular Detection Technology and Medicinal Effectiveness Appraisal, Zhejiang University, Hangzhou, China; MOE Frontier Science Center for Brain Science and Brain-machine Integration, Zhejiang University, Hangzhou, China. Electronic address: xukd@zju.edu.cn.

PMID: 36731770
DOI: 10.1016/j.brs.2023.01.1678

Abstract

Background: Modulation of brain circuits by electrical stimulation has led to exciting and powerful therapies for diseases such as Parkinson's. Because human brain organization is based in mesoscale (millimeter-scale) functional nodes, having a method that can selectively target such nodes could enable more precise, functionally specific stimulation therapies. Infrared Neural Stimulation (INS) is an emerging stimulation technology that stimulates neural tissue via delivery of tiny heat pulses. In nonhuman primates, this optical method provides focal intensity-dependent stimulation of the brain without tissue damage. However, whether INS application to the human central nervous system (CNS) is similarly effective is unknown.

Objective: To examine the effectiveness of INS on human cerebral cortex in intraoperative setting and to evaluate INS damage threshholds.

Methods: Five epileptic subjects undergoing standard lobectomy for epilepsy consented to this study. Cortical response to INS was assessed by intrinsic signal optical imaging (OI, a method that detects changes in tissue reflectance due to neuronal activity). A custom integrated INS and OI system was developed specifically for short-duration INS and OI acquisition during surgical procedures. Single pulse trains of INS with intensities from 0.2 to 0.8 J/cm² were delivered to the somatosensory cortex and responses were recorded via optical imaging. Following tissue resection, histological analysis was conducted to evaluate damage threshholds.

Results: As assessed by OI, and similar to results in monkeys, INS induced responses in human cortex were highly focal (millimeter sized) and led to relative suppression of nearby cortical sites. Intensity dependence was observed at both stimulated and functionally connected sites. Histological analysis of INS-stimulated human cortical tissue provided damage threshold estimates.

Conclusion: This is the first study demonstrating application of INS to human CNS and shows feasibility for stimulating single cortical nodes and associated sites and provided INS damage threshold estimates for cortical tissue. Our results suggest that INS is a promising tool for stimulation of functionally selective mesoscale circuits in the human brain, and may lead to advances in the future of precision medicine.

Keywords: Cerebral cortex; Cortical connections; Infrared neural stimulation; Optical imaging; Thermal damage.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Brain Mapping / methods
Brain*
Cerebral Cortex
Electric Stimulation / methods
Humans
Neurons* / physiology