Distinct patterns of metabolic motor cortex activity for phantom and residual limb pain in people with amputations: A functional near-infrared spectroscopy study

IF 2.7 4区 医学 Q2 CLINICAL NEUROLOGY Neurophysiologie Clinique/Clinical Neurophysiology Pub Date : 2024-02-01 DOI:10.1016/j.neucli.2023.102939
Marcel Simis , Lucas Murrins Marques , Sara Pinto Barbosa , André Tadeu Sugawara , João Ricardo Sato , Kevin Pacheco-Barrios , Linamara Rizzo Battistella , Felipe Fregni
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Abstract

Background

Phantom pain limb (PLP) has gained more attention due to the large number of people with amputations around the world and growing knowledge of the pain process, although its mechanisms are not completely understood.

Objectives

The aim of this study was to understand, in patients with amputations, the association between PLP and residual limb pain (RLP), and the brain metabolic response in cortical motor circuits, using functional near-infrared spectroscopy (fNIRS).

Methods

Sixty participants were recruited from the rehabilitation program in São Paulo, Brazil. Included patients were aged over 18 years, with traumatic unilateral lower-limb amputation, with PLP for at least 3 months after full recovery from amputation surgery. PLP and RLP levels were measured using visual analogue scales. fNIRS was performed during motor execution and motor mirror tasks for 20 s. In order to highlight possible variables related to variation in pain measures, univariate linear regression analyses were performed for both experimental conditions, resulting in four fNIRS variables (two hemispheres x two experimental conditions). Later, in order to test the topographic specificity of the models, eight multivariate regression analyses were performed (two pain scales x two experimental conditions x two hemispheres), including the primary motor cortex (PMC) related channel as an independent variable as well as five other channels related to the premotor area, supplementary area, and somatosensory cortex. All models were controlled for age, sex, ethnicity, and education.

Results

We found that: i) there is an asymmetric metabolic activation during motor execution and mirror task between hemispheres (with a predominance that is ipsilateral to the amputated limb), ii) increased metabolic response in the PMC ipsilateral to the amputation is associated with increased PLP (during both experimental tasks), while increased metabolic response in the contralateral PMC is associated with increased RLP (during the mirror motor task only); ii) increased metabolic activity of the ipsilateral premotor region is associated with increased PLP during the motor mirror task; iii) RLP was only associated with higher metabolic activity in the contralateral PMC and lower metabolic activity in the ipsilateral inferior frontal region during motor mirror task, but PLP was associated with higher metabolic activity during both tasks.

Conclusion

These results suggest there is both task and region specificity for the association between the brain metabolic response and the two different types of post-amputation pain. The metabolic predominance that is ipsilateral to the amputated limb during both tasks was associated with higher levels of PLP, suggesting a cortical motor network activity imbalance due to potential interhemispheric compensatory mechanisms. The present work contributes to the understanding of the underlying topographical patterns in the motor-related circuits associated with pain after amputations.

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截肢者幻肢痛和残肢痛的代谢运动皮层活动模式不同:功能性近红外光谱研究
背景幻肢痛(Phantom pain limb,PLP)由于全球截肢患者人数众多以及人们对疼痛过程的认识不断加深而受到越来越多的关注,尽管人们对其机制尚未完全了解。方法从巴西圣保罗的康复项目中招募了 60 名参与者。研究人员从巴西圣保罗的康复项目中招募了 60 名参与者,其中包括年龄超过 18 岁的外伤性单侧下肢截肢患者,以及在截肢手术完全康复后至少 3 个月仍有 PLP 的患者。为了突出与疼痛测量变化相关的可能变量,对两种实验条件进行了单变量线性回归分析,得出了四个 fNIRS 变量(两个半球 x 两个实验条件)。随后,为了测试模型的地形特异性,进行了八次多元回归分析(两个疼痛量表 x 两个实验条件 x 两个半球),包括作为自变量的初级运动皮层(PMC)相关通道以及与前运动区、辅助区和躯体感觉皮层相关的其他五个通道。所有模型均控制了年龄、性别、种族和教育程度。结果我们发现i) 在执行运动和镜像任务时,大脑半球之间的代谢激活不对称(以截肢同侧为主);ii) 截肢同侧运动前区代谢反应的增加与 PLP 的增加有关(在两项实验任务中),而对侧运动前区代谢反应的增加与 RLP 的增加有关(仅在镜像运动任务中);ii)在运动镜像任务中,同侧运动前区代谢活动的增加与 PLP 的增加有关;iii)在运动镜像任务中,RLP 仅与对侧运动前区代谢活动的增加有关,而与同侧额叶下区代谢活动的减少有关,但在两项任务中,PLP 都与代谢活动的增加有关。结论这些结果表明,大脑代谢反应与两种不同类型的截肢后疼痛之间存在任务和区域特异性。在这两项任务中,截肢肢体同侧的代谢优势与较高水平的 PLP 相关,这表明由于潜在的半球间补偿机制,大脑皮层运动网络活动失衡。本研究有助于了解与截肢后疼痛相关的运动相关回路的基本地形模式。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
CiteScore
5.20
自引率
3.30%
发文量
55
审稿时长
60 days
期刊介绍: Neurophysiologie Clinique / Clinical Neurophysiology (NCCN) is the official organ of the French Society of Clinical Neurophysiology (SNCLF). This journal is published 6 times a year, and is aimed at an international readership, with articles written in English. These can take the form of original research papers, comprehensive review articles, viewpoints, short communications, technical notes, editorials or letters to the Editor. The theme is the neurophysiological investigation of central or peripheral nervous system or muscle in healthy humans or patients. The journal focuses on key areas of clinical neurophysiology: electro- or magneto-encephalography, evoked potentials of all modalities, electroneuromyography, sleep, pain, posture, balance, motor control, autonomic nervous system, cognition, invasive and non-invasive neuromodulation, signal processing, bio-engineering, functional imaging.
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