Synchronization of somato-sympathetic outflows during exercise: role for a spinal rhythm generator.

Abstract

The synchronization of somatic motor outflow and sympathetic efferent activity during exercise has important functional consequences. For example, a certain degree of sympathetic vasoconstriction to active skeletal muscle vascular beds may be required to prevent an excessive decrease in vascular resistance during intense dynamic exercise involving a large skeletal muscle mass. Moreover, the redistribution of blood flow away from non-exercising vascular beds to contracting skeletal muscles is necessary to meet their increased metabolic demands. Historically, the nervous system has been separated arbitrarily into a volitional (somatic) and a reflex (autonomic) control system that does not necessitate volitional input (Koizumi & Brooks, 1972). However, during exercise this partition of the somatic and autonomic control systems is replaced by an overlapping control system that influences both somatic and sympathetic outflows in a parallel fashion. Previous work has suggested that the integration and co-ordination of the somatic and sympathetic motor responses during exercise were mediated by a supraspinal neural mechanism referred to as central command (Waldrop et al. 1996). However, there is an accumulating body of evidence, including papers on the role of the spinal cord in the regulation of sympathetic outflow (Weaver & Stein, 1989), suggesting that rhythmic neural activity destined for somatomotor and sympathetic outflows may be under the control of intrinsic neuronal circuitry in the spinal cord. In this issue of The Journal of Physiology, the paper by Chizh et al. (1998) demonstrates for the first time that some components of somatic motor and sympathetic neural outflows are synchronized by a spinal mechanism. The authors studied the relationship between sympathetic and somatic motor outflows from the thoraco-sacral spinal cord using an isolated trunk-hindquarters preparation of the adult mouse. They found that some of the activity in both somatic and sympathetic outflows was coupled. However, since there was also sympathetic neural activity that showed burst discharges in the absence of somatic motor activity, the spinal mechanism responsible for generating sympathetic burst activity was not the same mechanism that was responsible for somato-sympathetic coupling. Therefore, there remained spinal mechanisms that were capable of generating bursting activity independently of somatic and sympathetic activities. When NMDA was added to the perfusate to induce rhythmic somatic motor activity, a dose-dependent bursting pattern in sympathetic efferent and somatic motor nerves was evoked that was coupled at similar frequencies. Correlational analyses found a strong coherence between somatic motor outflow and sympathetic efferent discharge when triggered from peaks in somatic motor activity. However, this synchronization was not found when triggered from the peaks of sympathetic discharge. This finding led Chizh et al. (1998) to hypothesize that the generating mechanism responsible for somatic locomotor activity was the same mechanism responsible for coupling somatic outflow to sympathetic activity. These findings support the notion that the spinal cord possesses the necessary neuronal ‘machinery’ for generating and coupling sympathetic discharge with somatic motor outflow independently of supraspinal structures (i.e. the spinal rhythm generator represents a spinal central command). Important adjustments occur in the heart and blood vessels during exercise in order to provide the appropriate oxygen delivery to match the metabolic demand of contracting skeletal muscle. The coupling of somatic motor and sympathetic outflows is mediated by supraspinal neural mechanisms (supraspinal central command) in humans and animals (Fig. 1). In humans, intense intermittent static exercise produced a one-to-one synchronization of somatic motor activity with muscle sympathetic nerve activity that was purportedly directed to skeletal muscle vasculature (Victor et al. 1995). This synchronization persisted in the presence of both partial neuromuscular blockade (i.e. to increase central command) and after local anaesthetic block of the arm nerves to eliminate afferent feedback from skeletal muscle. Likewise, electrical and chemical stimulation of the hypothalamic locomotor region in decorticate cats after neuromuscular blockade evokes fictive locomotion that produces increases in arterial blood pressure (Waldrop et al. 1996) and synchronization of sympathetic nerve activity with hindlimb motor nerve activity (Hajduczok et al. 1991). And, as seen in humans, the synchronization of somatic motor activity and sympathetic discharge was unaffected by peripheral feedback mechanisms. These findings suggest that central command signals of supraspinal origin can regulate and co-ordinate sympathetic and somatomotor outflows during exercise. Figure 1 Synchronization of somatic motor outflow and sympathetic efferent activity during exercise is mediated by supraspinal and spinal mechanisms. The important work of Chizh et al. (1998) extends our understanding of the synchronization of somatic motor activity and sympathetic outflow by highlighting the role of a spinal somato-sympathetic generator (Fig. 1). Also, the coupling of somato-sympathetic neural outflows in the spinal cord may represent an exquisite mechanism to finely tune sympathetic discharge to the segmental level of somatic motor outflow during exercise. Finally, {fontsize the degree to which supraspinal central command signals influence the somato-sympathetic spinal generator needs to be studied to further our understanding of somato-sympathetic coupling during volitional exercise.