Elsevier

NeuroImage

Volume 128, March 2016, Pages 284-292
NeuroImage

Cortico-muscular synchronization by proprioceptive afferents from the tongue muscles during isometric tongue protrusion

https://doi.org/10.1016/j.neuroimage.2015.12.058Get rights and content

Highlights

  • MEG–EMG coherence was detected at 2–10 Hz and 15–35 Hz during tongue protrusion.

  • The MEG signal followed the EMG signal at 2–10 Hz, but preceded it at 15–35 Hz.

  • The source at 2–10 Hz was inferior to 15–35 Hz, and the same as tongue SEFs.

  • Coherence at 2–10 Hz reflects proprioceptive feedback from the tongue to cortex.

  • Such oscillatory feedback from the tongue may be important for human oral functions.

Abstract

Tongue movements contribute to oral functions including swallowing, vocalizing, and breathing. Fine tongue movements are regulated through efferent and afferent connections between the cortex and tongue. It has been demonstrated that cortico-muscular coherence (CMC) is reflected at two frequency bands during isometric tongue protrusions: the beta (β) band at 15–35 Hz and the low-frequency band at 2–10 Hz. The CMC at the β band (β-CMC) reflects motor commands from the primary motor cortex (M1) to the tongue muscles through hypoglossal motoneuron pools. However, the generator mechanism of the CMC at the low-frequency band (low-CMC) remains unknown. Here, we evaluated the mechanism of low-CMC during isometric tongue protrusion using magnetoencephalography (MEG). Somatosensory evoked fields (SEFs) were also recorded following electrical tongue stimulation. Significant low-CMC and β-CMC were observed over both hemispheres for each side of the tongue. Time-domain analysis showed that the MEG signal followed the electromyography signal for low-CMC, which was contrary to the finding that the MEG signal preceded the electromyography signal for β-CMC. The mean conduction time from the tongue to the cortex was not significantly different between the low-CMC (mean, 80.9 ms) and SEFs (mean, 71.1 ms). The cortical sources of low-CMC were located significantly posterior (mean, 10.1 mm) to the sources of β-CMC in M1, but were in the same area as tongue SEFs in the primary somatosensory cortex (S1). These results reveal that the low-CMC may be driven by proprioceptive afferents from the tongue muscles to S1, and that the oscillatory interaction was derived from each side of the tongue to both hemispheres. Oscillatory proprioceptive feedback from the tongue muscles may aid in the coordination of sophisticated tongue movements in humans.

Introduction

Sophisticated tongue movements play essential roles in vital oral functions such as speech articulation, mastication, swallowing, and airway patency. These fine tongue movements are accurately regulated by descending motor commands from the cortex to the tongue muscles and by afferent sensory feedback from the tongue muscles to the cortex. Such bi-directional functional connections between the cortex and muscles are mainly reflected in the cortico-muscular coherence (CMC) (Mima and Hallett, 1999, van Wijk et al., 2012).

The physiological interpretation of CMC varies according to the frequency band. The CMC in the beta (β) frequency band at 15–35 Hz (β-CMC) is generally thought to reflect the cortical interaction of motoneuron pools (Farmer et al., 1993, Mills and Schubert, 1995). Magnetoencephalography (MEG) and electroencephalography (EEG) studies have shown that the β-CMC is derived from the primary motor cortex (M1) and drives the muscle activities of the limbs and fingers through spinal motoneurons (MEG: Conway et al., 1995, Salenius et al., 1996, Salenius et al., 1997, Brown et al., 1998, Gross et al., 2000) (EEG: Halliday et al., 1998, Mima et al., 2000). In our previous MEG study (Maezawa et al., 2014c), in addition to finding that the β-CMC for the thumb occurred over the contralateral hemisphere, we also found that the CMC for the tongue was detected at two different frequency bands (the β band and a low-frequency band at 2–10 Hz) over both hemispheres during isometric tongue protrusion for each side of the tongue. We concluded that the β-CMC for the tongue reflects the descending motor commands from M1 bilaterally to each side of the tongue through hypoglossal motoneuron pools. However, the mechanism of the CMC at the low-frequency band (low-CMC) is still unclear.

Recent studies on cortico-kinematic coherence (CKC) using an accelerometer demonstrated that the primary sensorimotor cortex (SM1) is strongly coherent at the low frequency band during repetitive finger movements (Piitulainen et al., 2013a, Piitulainen et al., 2013b, Bourguignon et al., 2015). These studies suggest that the CKC at the low frequency band mainly reflects proprioceptive afferent input from muscle spindles to the contralateral SM1. Thus, as the human tongue muscles are rich in muscle spindles, the low-CMC for the tongue may be related to proprioceptive afferents from the tongue muscles.

The object of the present study was to investigate the generator mechanism of the low-CMC during human tongue protrusion using MEG. To do this, we first identified the conduction time of the low-CMC between the cortex and tongue, and compared it with the conduction times of the β-CMC and the somatosensory evoked fields (SEFs) following tongue stimulation. Second, we examined the location of the cortical sources for the low-CMC compared with the source locations of the β-CMC and tongue SEFs.

Section snippets

Subjects

Twenty-one right-handed healthy volunteers (14 men, 7 women; aged 20–37 years; mean age, 28.0 years) were studied. None of the subjects had a history of neurological or psychiatric disorders. Written informed consent was obtained from all subjects before they were included in the study. The protocol for this study was approved by the Ethical Committee of Dental Medicine of Hokkaido University. A portion of this study (β-CMC) has been reported previously using different analysis methods in 15

Coherence

Fig. 1 shows examples of the EMG signals from both sides of the tongue during tongue protrusion in subject 10. We could detect cyclical EMG activity of the tongue at the low-frequency band, and such cyclical EMG activity was synchronized between sides of the tongue.

Fig. 2 provides the power spectra of the MEG signal from the right sensorimotor cortex and of the EMG from the left side of the tongue in subject 10 during the tongue protrusion task. Distinct MEG peaks were detected at the

Discussion

The present study demonstrates that the generator mechanism of the tongue CMC differed depending on the frequency band (low-frequency band vs. β band) during isometric tongue protrusion in humans. The low-CMC reflects functional coupling related to proprioceptive feedback from the tongue muscles to the cortex, in contrast with the β-CMC, which reveals the efferent motor commands from the cortex to the tongue muscles.

Acknowledgments

This work was supported by Grants-in-Aid for Scientific Research (B)24300192 (TM), (C)23591488 (HS), and (C)25462883 (MF), and Grants-in-Aid for Young Scientists (B)25862071 (HM) from the Japan Society for the Promotion of Science.

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