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Vestibular stimulation-induced facilitation of cervical premotoneuronal systems in humans

View Article: PubMed Central - PubMed

ABSTRACT

It is unclear how descending inputs from the vestibular system affect the excitability of cervical interneurons in humans. To elucidate this, we investigated the effects of galvanic vestibular stimulation (GVS) on the spatial facilitation of motor-evoked potentials (MEPs) induced by combined pyramidal tract and peripheral nerve stimulation. To assess the spatial facilitation, electromyograms were recorded from the biceps brachii muscles (BB) of healthy subjects. Transcranial magnetic stimulation (TMS) over the contralateral primary motor cortex and electrical stimulation of the ipsilateral ulnar nerve at the wrist were delivered either separately or together, with interstimulus intervals of 10 ms (TMS behind). Anodal/cathodal GVS was randomly delivered with TMS and/or ulnar nerve stimulation. The combination of TMS and ulnar nerve stimulation facilitated BB MEPs significantly more than the algebraic summation of responses induced separately by TMS and ulnar nerve stimulation (i.e., spatial facilitation). MEP facilitation significantly increased when combined stimulation was delivered with GVS (p < 0.01). No significant differences were found between anodal and cathodal GVS. Furthermore, single motor unit recordings showed that the short-latency excitatory peak in peri-stimulus time histograms during combined stimulation increased significantly with GVS. The spatial facilitatory effects of combined stimulation with short interstimulus intervals (i.e., 10 ms) indicate that facilitation occurred at the premotoneuronal level in the cervical cord. The present findings therefore suggest that GVS facilitates the cervical interneuron system that integrates inputs from the pyramidal tract and peripheral nerves and excites motoneurons innervating the arm muscles.

No MeSH data available.


Related in: MedlinePlus

Schematic of the methodology and potential premotoneuronal pathways in the cervical cord.The wiring pattern is oversimplified for better understanding. Black and red solid lines represent direct (monosynaptic) connections, whereas purple and green dashed lines represent indirect (non-monosynaptic) connections no matter whether its effect is facilitatory or inhibitory. The pyramidal tract volleys (a red arrow) that are produced by transcranial magnetic stimulation (TMS) over the contralateral motor cortex and the afferent volleys (a green arrow) that are produced by electrical stimulation of the ipsilateral ulnar nerve (NERVE) at the wrist converge onto a common cervical interneuron (IN) that projects to motoneurons (MNs) of the biceps brachii (BB) muscle, which results in extra facilitation of motor-evoked potentials (MEPs) in the BB. The TMS and NERVE are timed so that the pyramidal tract and afferent volleys simultaneously arrive at the upper cervical cord. The inputs produced by galvanic vestibular stimulation (GVS) through the bilateral mastoid processes also converge on the IN pool. FDI: first dorsal interosseous muscle, EMG: electromyogram.
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pone.0175131.g002: Schematic of the methodology and potential premotoneuronal pathways in the cervical cord.The wiring pattern is oversimplified for better understanding. Black and red solid lines represent direct (monosynaptic) connections, whereas purple and green dashed lines represent indirect (non-monosynaptic) connections no matter whether its effect is facilitatory or inhibitory. The pyramidal tract volleys (a red arrow) that are produced by transcranial magnetic stimulation (TMS) over the contralateral motor cortex and the afferent volleys (a green arrow) that are produced by electrical stimulation of the ipsilateral ulnar nerve (NERVE) at the wrist converge onto a common cervical interneuron (IN) that projects to motoneurons (MNs) of the biceps brachii (BB) muscle, which results in extra facilitation of motor-evoked potentials (MEPs) in the BB. The TMS and NERVE are timed so that the pyramidal tract and afferent volleys simultaneously arrive at the upper cervical cord. The inputs produced by galvanic vestibular stimulation (GVS) through the bilateral mastoid processes also converge on the IN pool. FDI: first dorsal interosseous muscle, EMG: electromyogram.

Mentions: The test sequences consisted of three types of stimulus trials: (1) separate ulnar nerve stimulation, (2) separate TMS, and (3) combined ulnar nerve stimulation and TMS. For the combined stimulation, a 10-ms inter-stimulus interval (ISI) was used, with ulnar nerve stimulation delivered before the TMS. The rationale for the use of this ISI was based on the findings of our preliminary experiments on 5 subjects that showed that the combination of TMS and ulnar nerve stimulation with a 10-ms ISI efficiently facilitated the MEPs compared with stimulations with other ISIs (i.e., 6, 7, 7.5, 8, 9, 11, 12, and 15-ms ISIs) in all of the subjects. Based on the results of previous studies, the conduction time was estimated such that the afferent time from the wrist to the upper cervical cord (green arrow in Fig 2) and the efferent time from the motor cortex to the cervical cord (red arrow in Fig 2) were ~14 ms [30, 31] and 3.6–4 ms [32], respectively. Thus, a 10-ms ISI, together with analyses of short latency effects starting around MEP onset, allowed us to investigate the effects of the simultaneous convergence of inputs from the ulnar nerve at the wrist level and the pyramidal tract onto cervical INs. The three types of stimulus trials were randomly delivered with intertrial intervals of 4–6 s in the MEP-recording experiments and 2–3 s in the MU-recording experiments. The number of stimuli in each stimulus condition was 10 stimuli for the MEP-recording experiments and 50 stimuli for the MU-recording experiments. In the MEP-recording experiments, three test sequences were performed under different GVS conditions, i.e., without (control) and with anodal or cathodal GVS. Because no significant differences were found between anodal and cathodal GVS, we focused on the control and anodal GVS conditions in the MU-recording experiments in order to complete the recordings from the same MU in minimal time. In the GVS conditions, the TMS was delivered 0.5 s after the beginning of the GVS pulse. The long ISI in the GVS was selected in order to avoid any confounding ON/OFF effects of the GVS itself on the background EMG activity [15, 16, 33]. The orders of the test sequences were randomized.


Vestibular stimulation-induced facilitation of cervical premotoneuronal systems in humans
Schematic of the methodology and potential premotoneuronal pathways in the cervical cord.The wiring pattern is oversimplified for better understanding. Black and red solid lines represent direct (monosynaptic) connections, whereas purple and green dashed lines represent indirect (non-monosynaptic) connections no matter whether its effect is facilitatory or inhibitory. The pyramidal tract volleys (a red arrow) that are produced by transcranial magnetic stimulation (TMS) over the contralateral motor cortex and the afferent volleys (a green arrow) that are produced by electrical stimulation of the ipsilateral ulnar nerve (NERVE) at the wrist converge onto a common cervical interneuron (IN) that projects to motoneurons (MNs) of the biceps brachii (BB) muscle, which results in extra facilitation of motor-evoked potentials (MEPs) in the BB. The TMS and NERVE are timed so that the pyramidal tract and afferent volleys simultaneously arrive at the upper cervical cord. The inputs produced by galvanic vestibular stimulation (GVS) through the bilateral mastoid processes also converge on the IN pool. FDI: first dorsal interosseous muscle, EMG: electromyogram.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5384664&req=5

pone.0175131.g002: Schematic of the methodology and potential premotoneuronal pathways in the cervical cord.The wiring pattern is oversimplified for better understanding. Black and red solid lines represent direct (monosynaptic) connections, whereas purple and green dashed lines represent indirect (non-monosynaptic) connections no matter whether its effect is facilitatory or inhibitory. The pyramidal tract volleys (a red arrow) that are produced by transcranial magnetic stimulation (TMS) over the contralateral motor cortex and the afferent volleys (a green arrow) that are produced by electrical stimulation of the ipsilateral ulnar nerve (NERVE) at the wrist converge onto a common cervical interneuron (IN) that projects to motoneurons (MNs) of the biceps brachii (BB) muscle, which results in extra facilitation of motor-evoked potentials (MEPs) in the BB. The TMS and NERVE are timed so that the pyramidal tract and afferent volleys simultaneously arrive at the upper cervical cord. The inputs produced by galvanic vestibular stimulation (GVS) through the bilateral mastoid processes also converge on the IN pool. FDI: first dorsal interosseous muscle, EMG: electromyogram.
Mentions: The test sequences consisted of three types of stimulus trials: (1) separate ulnar nerve stimulation, (2) separate TMS, and (3) combined ulnar nerve stimulation and TMS. For the combined stimulation, a 10-ms inter-stimulus interval (ISI) was used, with ulnar nerve stimulation delivered before the TMS. The rationale for the use of this ISI was based on the findings of our preliminary experiments on 5 subjects that showed that the combination of TMS and ulnar nerve stimulation with a 10-ms ISI efficiently facilitated the MEPs compared with stimulations with other ISIs (i.e., 6, 7, 7.5, 8, 9, 11, 12, and 15-ms ISIs) in all of the subjects. Based on the results of previous studies, the conduction time was estimated such that the afferent time from the wrist to the upper cervical cord (green arrow in Fig 2) and the efferent time from the motor cortex to the cervical cord (red arrow in Fig 2) were ~14 ms [30, 31] and 3.6–4 ms [32], respectively. Thus, a 10-ms ISI, together with analyses of short latency effects starting around MEP onset, allowed us to investigate the effects of the simultaneous convergence of inputs from the ulnar nerve at the wrist level and the pyramidal tract onto cervical INs. The three types of stimulus trials were randomly delivered with intertrial intervals of 4–6 s in the MEP-recording experiments and 2–3 s in the MU-recording experiments. The number of stimuli in each stimulus condition was 10 stimuli for the MEP-recording experiments and 50 stimuli for the MU-recording experiments. In the MEP-recording experiments, three test sequences were performed under different GVS conditions, i.e., without (control) and with anodal or cathodal GVS. Because no significant differences were found between anodal and cathodal GVS, we focused on the control and anodal GVS conditions in the MU-recording experiments in order to complete the recordings from the same MU in minimal time. In the GVS conditions, the TMS was delivered 0.5 s after the beginning of the GVS pulse. The long ISI in the GVS was selected in order to avoid any confounding ON/OFF effects of the GVS itself on the background EMG activity [15, 16, 33]. The orders of the test sequences were randomized.

View Article: PubMed Central - PubMed

ABSTRACT

It is unclear how descending inputs from the vestibular system affect the excitability of cervical interneurons in humans. To elucidate this, we investigated the effects of galvanic vestibular stimulation (GVS) on the spatial facilitation of motor-evoked potentials (MEPs) induced by combined pyramidal tract and peripheral nerve stimulation. To assess the spatial facilitation, electromyograms were recorded from the biceps brachii muscles (BB) of healthy subjects. Transcranial magnetic stimulation (TMS) over the contralateral primary motor cortex and electrical stimulation of the ipsilateral ulnar nerve at the wrist were delivered either separately or together, with interstimulus intervals of 10 ms (TMS behind). Anodal/cathodal GVS was randomly delivered with TMS and/or ulnar nerve stimulation. The combination of TMS and ulnar nerve stimulation facilitated BB MEPs significantly more than the algebraic summation of responses induced separately by TMS and ulnar nerve stimulation (i.e., spatial facilitation). MEP facilitation significantly increased when combined stimulation was delivered with GVS (p < 0.01). No significant differences were found between anodal and cathodal GVS. Furthermore, single motor unit recordings showed that the short-latency excitatory peak in peri-stimulus time histograms during combined stimulation increased significantly with GVS. The spatial facilitatory effects of combined stimulation with short interstimulus intervals (i.e., 10 ms) indicate that facilitation occurred at the premotoneuronal level in the cervical cord. The present findings therefore suggest that GVS facilitates the cervical interneuron system that integrates inputs from the pyramidal tract and peripheral nerves and excites motoneurons innervating the arm muscles.

No MeSH data available.


Related in: MedlinePlus