Legon Wynn, Strohman Andrew, In Alexander, Stebbins Katelyn, Payne Brighton
Fralin Biomedical Research Institute at Virginia Tech Carilion, Roanoke, VA, 24016, USA.
School of Neuroscience, Virginia Polytechnic Institute and State University, Blacksburg, VA, 24061, USA.
bioRxiv. 2023 May 5:2023.05.05.539593. doi: 10.1101/2023.05.05.539593.
The insula is a portion of the cerebral cortex folded deep within the lateral sulcus covered by the overlying opercula of the inferior frontal lobe and superior portion of the temporal lobe. The insula has been parsed into sub-regions based upon cytoarchitectonics and structural and functional connectivity with multiple lines of evidence supporting specific roles for each of these sub-regions in pain processing and interoception. In the past, causal interrogation of the insula was only possible in patients with surgically implanted electrodes. Here, we leverage the high spatial resolution combined with the deep penetration depth of low-intensity focused ultrasound (LIFU) to non-surgically modulate either the anterior insula (AI) or posterior insula (PI) in humans for effect on subjective pain ratings, electroencephalographic (EEG) contact head evoked potentials (CHEPs) and time-frequency power as well as autonomic measures including heart-rate variability (HRV) and electrodermal response (EDR). N = 23 healthy volunteers received brief noxious heat pain stimuli to the dorsum of their right hand during continuous heart-rate, EDR and EEG recording. LIFU was delivered to either the AI (anterior short gyrus), PI (posterior longus gyrus) or under an inert sham condition time-locked to the heat stimulus. Results demonstrate that single-element 500 kHz LIFU is capable of individually targeting specific gyri of the insula. LIFU to both AI and PI similarly reduced perceived pain ratings but had differential effects on EEG activity. LIFU to PI affected earlier EEG amplitudes around 300 milliseconds whereas LIFU to AI affected EEG amplitudes around 500 milliseconds. In addition, only LIFU to the AI affected HRV as indexed by an increase in standard deviation of N-N intervals (SDNN) and mean HRV low frequency power. There was no effect of LIFU to either AI or PI on EDR or blood pressure. Taken together, LIFU looks to be an effective method to individually target sub-regions of the insula in humans for site-specific effects on brain biomarkers of pain processing and autonomic reactivity that translates to reduced perceived pain to a transient heat stimulus. These data have implications for the treatment of chronic pain and several neuropsychological diseases like anxiety, depression and addiction that all demonstrate abnormal activity in the insula concomitant with dysregulated autonomic function.
脑岛是大脑皮层的一部分,折叠于外侧沟深处,被额叶下回和颞叶上部的覆盖脑回所覆盖。基于细胞结构以及与多个区域的结构和功能连接,脑岛已被划分为不同的亚区域,多条证据支持这些亚区域在疼痛处理和内感受中发挥特定作用。过去,只有通过手术植入电极的患者才能对脑岛进行因果性研究。在此,我们利用低强度聚焦超声(LIFU)的高空间分辨率和深穿透深度,以非手术方式调节人类的前脑岛(AI)或后脑岛(PI),以观察其对主观疼痛评分、脑电图(EEG)接触性头部诱发电位(CHEP)和时频功率的影响,以及对包括心率变异性(HRV)和皮肤电反应(EDR)在内的自主神经指标的影响。23名健康志愿者在连续记录心率、EDR和EEG的过程中,右手背部接受短暂的有害热痛刺激。LIFU分别作用于AI(前短回)、PI(后长回)或在惰性假刺激条件下,与热刺激进行时间锁定。结果表明,单元素500kHz的LIFU能够分别靶向脑岛的特定脑回。对AI和PI施加LIFU同样降低了疼痛评分,但对EEG活动有不同影响。对PI施加LIFU影响约300毫秒时的早期EEG振幅,而对AI施加LIFU影响约500毫秒时的EEG振幅。此外,只有对AI施加LIFU会影响HRV,表现为N-N间期标准差(SDNN)增加和平均HRV低频功率增加。对AI或PI施加LIFU对EDR或血压均无影响。综上所述,LIFU似乎是一种有效的方法,可以分别靶向人类脑岛的亚区域,对疼痛处理和自主神经反应的脑生物标志物产生位点特异性影响,从而减轻对短暂热刺激的疼痛感受。这些数据对慢性疼痛以及焦虑、抑郁和成瘾等几种神经心理疾病的治疗具有启示意义,这些疾病均表现为脑岛活动异常并伴有自主神经功能失调。