Sympathetic Neuronal Oscillators are Capable of Dynamic Synchronization

Abstract

In this paper we show that the discharges of sympathetic neurons innervating an identified peripheral target are driven by multiple oscillators that undergo dynamic synchronization when an entraining force, central respiratory drive (CRD), is increased. Activity was recorded from postganglionic sympathetic neurons (PGNs) innervating the caudal ventral artery of the rat tail: (1) at the population level from the ventral collector nerve (VCN); and (2) from pairs of single PGNs recorded simultaneously using a focal recording technique. Autospectral analysis of VCN activity revealed a more prominent rhythmical component in the presence of CRD than in its absence, suggesting that (1) multiple oscillators drive the discharges of PGNs and (2) these oscillators can be entrained and therefore synchronized by CRD. This interpretation was supported by analysis of the firing behavior of PGN pairs. Autocorrelation and cross-correlation analysis showed that pairs were not synchronized in the absence of CRD but showed significant synchronization when CRD was enhanced. Time-evolving spectral analysis and raster plots demonstrated that the temporal stability of PGN-to-PGN and CRD-to-PGN interactions at a given level of CRD were also dynamic in nature, with stable constant phase relationships predominating as CRD was increased. This is the first reported example of dynamic synchronization in populations of single postganglionic sympathetic neurons, and we suggest that, as in sensory processing and motor control, temporal pattern coding may also be an important feature of neuronal discharges in sympathetic pathways.

Electrophysiological properties of electrical synapses between rat sympathetic preganglionic neurones in vitro

“…Synchronisation of activity between SPNs appears to involve reliable, reciprocal communication of sub-and suprathreshold neuronal activity by electrical synapses, with firing of action potentials by one or a small number of presynaptic neurones being sufficient to drive synchronisation of activity between adjoining neurones. The low-pass filter characteristics of these synapses suggest a cellular mechanism which may promote expression of relatively low frequency synchronised sympathetic rhythms, for example those recorded from the caudal ventral artery of the tail (Johnson & Gilbey, 1996;Chang et al 1999). Bennett, M. V. L. (1966).…”

What can we learn about neural control of the cardiovascular system by studying rhythms in sympathetic nerve activity?

“…Three, the synchronous bursts of SNA do not look like simple sine waves; rather the duration and interval between bursts are quite variable, especially after baroreceptor denervation. Indeed, central sympathetic circuits are dynamic and can generate different burst patterns depending on the physiological state of the animal, the type of nerve being studied, as well as the species (Barman and Gebber, 2000; Barman and Kenney, 2007; Chang et al, 1999; Charkoudian and Wallin, 2014; Hashimoto et al, 1999; Malpas, 1998, 2010). …”

“…Although most recognized for having cardiac-related and respiratory-related discharges, sympathetic neural networks are quite complex and generate a variety of periodicities that range between ~0.04 and 10 Hz or even higher, and even diurnal variations, depending on the physiological or pathophysiological conditions, type of nerve being analyzed, age of the subject, and the species (Barman and Gebber, 2000; Barman and Kenney, 2007; Chang et al, 1999; Charkoudian and Wallin, 2014; Hashimoto et al, 1999; Malpas, 1998, 2010; Narkiewicz et al, 2002). …”

Landmarks in understanding the central nervous control of the cardiovascular system

“…Thus, sympathetic vasomotor nerves supplying different vascular beds display different basic rhythms, supporting the concept of multiple oscillators (Gebber et al 1994 a ; Gilbey, 2001). Further support for the idea of oscillating networks was provided by evidence showing that the fundamental rhythm can be entrained by afferent input from arterial baroreceptors, central respiratory drive and lung inflation, provided that the frequency of the input is close to the uncoupled frequency of the discharge (Gebber et al 1994 a ; Zhang et al 1997; Johnson & Gilbey, 1998; Chong et al 1999; Staras et al 2001). This is unlikely to be a characteristic of pacemaker neurones, since they would reset to the same rhythm after each stimulus.…”