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