Heart Rate Changes in Response to Mechanical Pressure Stimulation of Skeletal Muscles Are Mediated by Cardiac Sympathetic Nerve Activity.

Nobuhiro Watanabe,Harumi Hotta

doi:10.3389/fnins.2016.00614

Abstract

Stimulation of mechanoreceptors in skeletal muscles such as contraction and stretch elicits reflexive autonomic nervous system changes which impact cardiovascular control. There are pressure-sensitive mechanoreceptors in skeletal muscles. Mechanical pressure stimulation of skeletal muscles can induce reflex changes in heart rate (HR) and blood pressure, although the neural mechanisms underlying this effect are unclear. We examined the contribution of cardiac autonomic nerves to HR responses induced by mechanical pressure stimulation (30 s, ~10 N/cm2) of calf muscles in isoflurane-anesthetized rats. Animals were artificially ventilated and kept warm using a heating pad and lamp, and respiration and core body temperature were maintained within physiological ranges. Mechanical stimulation was applied using a stimulation probe 6 mm in diameter with a flat surface. Cardiac sympathetic and vagus nerves were blocked to test the contribution of the autonomic nerves. For sympathetic nerve block, bilateral stellate ganglia, and cervical sympathetic nerves were surgically sectioned, and for vagus nerve block, the nerve was bilaterally severed. In addition, mass discharges of cardiac sympathetic efferent nerve were electrophysiologically recorded. Mechanical stimulation increased or decreased HR in autonomic nerve-intact rats (range: −56 to +10 bpm), and the responses were negatively correlated with pre-stimulus HR (r = −0.65, p = 0.001). Stimulation-induced HR responses were markedly attenuated by blocking the cardiac sympathetic nerve (range: −9 to +3 bpm, p < 0.0001) but not the vagus nerve (range: −75 to +30 bpm, p = 0.17). In the experiments with cardiac sympathetic efferent nerve activity recordings, mechanical stimulation increased, or decreased the frequency of sympathetic nerve activity in parallel with HR (r = 0.77, p = 0.0004). Furthermore, the changes in sympathetic nerve activity were negatively correlated with its tonic level (r = −0.62, p = 0.0066). These results suggest that cardiac sympathetic nerve activity regulates HR responses to muscle mechanical pressure stimulation and the direction of HR responses depends on the tonic level of the nerve activity, i.e., bradycardia occurs when the tonic activity is high and tachycardia occurs when the activity is low.

Highlights

Somatosensory stimulation reflexively elicits autonomic nervous activity changes and affects cardiovascular control in anesthetized animals, in whom consciousness and emotions that are potentially influential are eliminated by the administration of anesthesia (Sato et al, 1997; Watanabe et al, 2015)
The present results demonstrate that (1) calf muscle pressure stimulation induces tachycardiac or bradycardiac responses by regulating cardiac sympathetic efferent nerve activity response (CSNA) because heart rate (HR) responses to pressure stimulation in cardiac sympathetic nerve blocked condition were marginal and the direction of the HR change paralleled that of CSNA and
HR Responses to Mechanical Pressure Stimulation of the Calf Muscle Were Mediated by Cardiac Sympathetic Nerves

Summary

INTRODUCTION

Somatosensory stimulation reflexively elicits autonomic nervous activity changes and affects cardiovascular control (somatocardiovascular reflexes) in anesthetized animals, in whom consciousness and emotions that are potentially influential are eliminated by the administration of anesthesia (Sato et al, 1997; Watanabe et al, 2015). Even under controlled experimental conditions, it was reported that electrical stimulation of muscle afferents (Sato et al, 1981), bradykinin infusion to hindlimb muscles (Sato et al, 1982), and acupuncture-like stimulation to hindlimb muscles (Ohsawa et al, 1995) could induce tachycardiac and bradycardiac or pressor and depressor responses The reasons for these bidirectional cardiovascular responses have not been studied. To maintain the constant level of anesthesia through data recordings, we used inhalation anesthesia (isoflurane) in the present study

MATERIALS AND METHODS

RESULTS

DISCUSSION