Transcallosal connections of face and hand representation areas in the primary motor cortex: a transcranial magnetic stimulation and transcranial magnetic stimulation–electroencephalography study

IF 4.4 2区 医学 Q1 NEUROSCIENCES Journal of Physiology-London Pub Date : 2025-02-09 DOI:10.1113/JP286473
Francesca Ginatempo, Elias P. Casula, Giulia Soggia, Nicola Loi, Mohammed Zeroual, Franca Deriu
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Abstract

Conflictual anatomical and neurophysiological findings obtained in both primates and humans raised the question whether the transcallosal pathway connecting the two representation areas of the face in the primary motor cortex (fM1) is absent or present but weak and poorly active. To answer this question in the present study transcranial magnetic stimulation (TMS) and electroencephalography (EEG) were combined as the TMS–EEG approach to investigate the transcallosal pathway connecting fM1s from both a spatial and a functional point of view. For comparison the same approach was used in hand M1 (hM1). Eighteen healthy subjects underwent two experimental sessions where both hemispheres were investigated: (1) a TMS session, to evaluate interhemispheric inhibition (IHI) for the depressor anguli oris (DAO) and the first dorsal interosseus (FDI) M1 representations, and (2) a TMS–EEG session, to calculate the interhemispheric signal propagation (ISP) for the DAO area in fM1 and the FDI area in hM1. Results found the presence of IHI for hM1 and its absence for fM1. On the contrary ISP analysis demonstrated a significant suppression of activity in the non-stimulated hemisphere compared to the stimulated one, with no difference between the stimulated hemisphere and the representation area. Finally a significant correlation was detected between IHI and ISP only when stimulating the left hM1. Overall the present study suggests the presence of a transcallosal connection between the two fM1s in humans, as demonstrated by the ISP analysis. This interhemispheric connection is however functionally poorly active, as demonstrated by the lack of IHI.

Key points

  • Although the transcallosal connection between hand primary motor cortices (M1) is functionally powerful, to allow hand asymmetrical movements, its role in face motor control is controversial. Indeed to produce face expressions, face muscles are rarely involved symmetrically, and their face M1 control is bilateral and lacks interhemispheric inhibition (IHI).
  • We investigated the transcallosal connection between face M1s, and for comparison in hand M1 (hM1), both spatially and functionally using transcranial magnetic stimulation (TMS) to study IHI, and electroencephalography (EEG) combined with TMS, to study interhemispheric signal propagation.
  • Functional IHI data confirmed its absence in face M1 and its presence in hM1.
  • In contrast TMS–EEG spatial analysis demonstrated a significant inhibition of activity in the non-stimulated hemisphere, regardless of the cortical area.
  • Face M1s are connected by a transcallosal pathway, which is poorly active in physiological conditions. In addition no clear hemispheric dominance exists in face cortical control.

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初级运动皮层中面部和手部表征区的经胼胝体连接:经颅磁刺激和经颅磁刺激-脑电图研究。
在灵长类动物和人类身上获得的解剖学和神经生理学研究结果存在冲突,这就提出了一个问题,即连接初级运动皮层(fM1)中脸部两个表征区域的跨胼胝体通路是不存在还是存在但功能弱且活性差。为了回答这个问题,本研究采用经颅磁刺激(TMS)和脑电图(EEG)相结合的 TMS-EEG 方法,从空间和功能角度研究连接 fM1 的跨胼胝体通路。为了进行比较,同样的方法也用于手部 M1(hM1)。18 名健康受试者接受了两个实验环节,对两个半球进行了调查:(1) TMS 环节,用于评估眼下皱襞(DAO)和第一背侧骨间(FDI)M1 表征的半球间抑制(IHI);(2) TMS-EEG 环节,用于计算 fM1 的 DAO 区域和 hM1 的 FDI 区域的半球间信号传播(ISP)。结果发现 hM1 存在 IHI,而 fM1 则不存在。相反,ISP 分析表明,与受刺激半球相比,未受刺激半球的活动明显受到抑制,而受刺激半球与代表区之间没有差异。最后,只有在刺激左侧 hM1 时,才能发现 IHI 和 ISP 之间存在明显的相关性。总体而言,本研究表明,正如 ISP 分析所证明的那样,人类的两个 fM1 之间存在着跨胼胝体的联系。然而,正如缺乏 IHI 所证明的那样,这种半球间连接在功能上并不活跃。要点:虽然手部初级运动皮层(M1)之间的跨胼胝体连接具有强大的功能,可以实现手部的不对称运动,但它在面部运动控制中的作用却存在争议。事实上,在制作面部表情时,面部肌肉很少对称参与,其面部 M1 控制是双侧的,缺乏半球间抑制(IHI)。我们利用经颅磁刺激(TMS)来研究 IHI,并结合脑电图(EEG)来研究半球间信号传播,从而研究了脸部 M1 与手部 M1(hM1)在空间和功能上的跨胼胝体连接。功能性 IHI 数据证实其在面 M1 中不存在,而在 hM1 中存在。相反,TMS-EEG 空间分析表明,无论在哪个皮层区域,未受刺激半球的活动都会受到显著抑制。面部 M1 由一条跨胼胝体通路连接,该通路在生理条件下的活性很差。此外,脸部皮质控制并不存在明显的半球优势。
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来源期刊
Journal of Physiology-London
Journal of Physiology-London 医学-神经科学
CiteScore
9.70
自引率
7.30%
发文量
817
审稿时长
2 months
期刊介绍: The Journal of Physiology publishes full-length original Research Papers and Techniques for Physiology, which are short papers aimed at disseminating new techniques for physiological research. Articles solicited by the Editorial Board include Perspectives, Symposium Reports and Topical Reviews, which highlight areas of special physiological interest. CrossTalk articles are short editorial-style invited articles framing a debate between experts in the field on controversial topics. Letters to the Editor and Journal Club articles are also published. All categories of papers are subjected to peer reivew. The Journal of Physiology welcomes submitted research papers in all areas of physiology. Authors should present original work that illustrates new physiological principles or mechanisms. Papers on work at the molecular level, at the level of the cell membrane, single cells, tissues or organs and on systems physiology are all acceptable. Theoretical papers and papers that use computational models to further our understanding of physiological processes will be considered if based on experimentally derived data and if the hypothesis advanced is directly amenable to experimental testing. While emphasis is on human and mammalian physiology, work on lower vertebrate or invertebrate preparations may be suitable if it furthers the understanding of the functioning of other organisms including mammals.
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