Human sympathetic outflows to skin and muscle target organs fluctuate concordantly over a wide range of time-varying frequencies

Bernjak, Alan and Cui, Jian and Iwase, Satoshi and Mano, Tadaaki and Stefanovska, Aneta and Eckberg, Dwain (2012) Human sympathetic outflows to skin and muscle target organs fluctuate concordantly over a wide range of time-varying frequencies. The Journal of Physiology, 590 (2). pp. 363-375. ISSN 0022-3751

Abstract

Non-technical summary  Traffic carried over two branches of the sympathetic nervous system can be recorded in cooperative human subjects, with fine needles inserted directly into leg nerves. We made simultaneous recordings of sympathetic activity with two needles inserted into nerve tracts supplying skin and muscles, and used a mathematical method, wavelet phase coherence, to obtain insights into how the brain regulates neural oscillations. Our results document continuously varying and coherently coupled human skin and muscle sympathetic nerve oscillations over time (suggesting that they are driven by other central frequency generators). Abstract  Frequency-domain analyses of simultaneously recorded skin and muscle sympathetic nerve activities may yield unique information on otherwise obscure central processes governing human neural outflows. We used wavelet transform and wavelet phase coherence methods to analyse integrated skin and muscle sympathetic nerve activities and haemodynamic fluctuations, recorded from nine healthy supine young men. We tested two null hypotheses: (1) that human skin and muscle sympathetic nerve activities oscillate congruently; and (2) that whole-body heating affects these neural outflows and their haemodynamic consequences in similar ways. Measurements included peroneal nerve skin and tibial nerve muscle sympathetic activities; the electrocardiogram; finger photoplethysmographic arterial pressure; respiration (controlled at 0.25 Hz, and registered with a nasal thermistor); and skin temperature, sweating, and laser-Doppler skin blood flow. We made recordings at ∼27°C, for ∼20 min, and then during room temperature increases to ∼38°C, over 35 min. We analysed data with a wavelet transform, using the Morlet mother wavelet and wavelet phase coherence, to determine the frequencies and coherences of oscillations over time. At 27°C, skin and muscle nerve activities oscillated coherently, at ever-changing frequencies between 0.01 and the cardiac frequency (∼1 Hz). Heating significantly augmented oscillations of skin sympathetic nerve activity and skin blood flow, arterial pressure, and R-R intervals, over a wide range of low frequencies, and modestly reduced coordination between skin and muscle sympathetic oscillations. These results suggest that human skin and muscle sympathetic motoneurones are similarly entrained by external influences, including those of arterial baroreceptors, respiration, and other less well-defined brainstem oscillators. Our study provides strong support for the existence of multiple, time-varying central sympathetic neural oscillators in human subjects.