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

• Published in: The Journal of physiology Vol. 603; no. 5; pp. 1225 - 1240
• Main Authors: Ginatempo, Francesca, Casula, Elias P., Soggia, Giulia, Loi, Nicola, Zeroual, Mohammed, Deriu, Franca
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 01.03.2025
• Subjects: Adult; Cerebral hemispheres; Corpus Callosum - physiology; Cortex (motor); EEG; Electroencephalography; Evoked Potentials, Motor; Face; Face - innervation; Face - physiology; face primary motor cortex; Female; Hand - innervation; Hand - physiology; Humans; interhemispheric inhibition; interhemispheric signal propagation; Magnetic fields; Male; Motor Cortex - physiology; Motor task performance; Muscles; transcallosal pathway; Transcranial Magnetic Stimulation; transcranial magnetic stimulation (TMS)‐evoked potentials; Young Adult; interhemispheric signal propagation; interhemispheric inhibition; face primary motor cortex; transcallosal pathway; transcranial magnetic stimulation (TMS)‐evoked potentials
• ISSN: 0022-3751; 1469-7793; 1469-7793
• DOI: 10.1113/JP286473

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. figure legend Transcallosal connections through the two representation areas of the face in the primary motor cortex (M1) of humans have been questioned by previous works, differently from those connecting hand M1s (hM1s), which are well known instead. This study explored the transcallosal pathway connecting face M1s and hM1s from both spatial and functional points of view using transcranial magnetic stimulation (TMS) protocols investigating interhemispheric inhibition (IHI) and electroencephalography combined with TMS to evaluate interhemispheric signal propagation (ISP). Data showed that IHI is absent in face M1 but present in hM1, whereas ISP was clearly detected in both face M1 and hM1 representation areas. Although confirming the strong interhemispheric connection between hM1s, which is essential to allow asymmetric hand movements, these novel results evidence that although a trancallosal connection exists between face M1s, it is functionally weak, probably because face muscles are hardly never involved in asymmetrical movements in physiological conditions.