Central visceral commands formatted as the slow rhythms encoded in the temporal structures of the sympathetic firing originated from the neonatal rat spinal cord in vitro

Abstract

Central sympathetic neural circuits continuously generate efferent commands to sustain rhythmic operations of their peripheral effectors. However, beyond the firing rates, in what configuration an effective visceral command is formatted by the spiking activities was largely unknown. This study used an in vitro splanchnic nerve-spinal cord preparation of the neonatal rats as an experimental model and recorded spontaneous efferent activities from single sympathetic fibers. The patterns of the fiber activities were quantitatively evaluated by a metric, the so-called local variation (Lv). Lv was derived from calculating the relative differences between adjacent interspike intervals (ISIs), and thus, described the spiking patterns from a regular spiking with Lv = 0 to that spiking in bursts with Lv >1. Along the time course, the dynamic components of Lv (dLv) displayed quasiperiodic oscillations. Continuous wavelet analysis showed that dLv oscillations registered a dominant power rhythm at [~]7 mHz. This slow rhythmicity was heterogeneously altered by application of various antagonists that interrupted endogenous neurotransmitter activities mediated by ionotropic glutamate receptors or GABAA receptors in the spinal cord. Thus, the oscillation of dLv manifested itself as a feature of neural network operation. On the assumption that the total power of the dLv oscillations reflects an activity status of neural network operation, the antagonist-induced change of the power fits well with a concomitant ISI change in a negative sigmoid relationship, which explains the heterogeneity of the antagonist-induced firing responses. In conclusion, dLv oscillations reflect a dynamic status of neural network operation. The slow rhythms embedded in the dLv oscillations are likely acting as an information coder and convey effective central visceral commands that can be followed by their downstream effectors. Author summaryIn what format the information is encoded by the neural activity is relatively unknown. This is especially true for autonomic regulation of visceral functions. We seek to determine the format of the central sympathetic commands, by which it can generate an effective driving force to regulate the operation of their peripheral target organs. Because most visceral organs operate with certain rhythms, we anticipate that the central visceral commands are also formatted in rhythms. Two aspects of techniques were employed. One was the in vitro electrophysiological and pharmacological techniques to acquire and to manipulate the neural signals recorded from sympathetic single-fibers. The other was the computational techniques to extract the information embedded in the timing of the spiking behaviors and to examine how these features were altered by pharmacological manipulations. We found a spontaneous change of sympathetic spiking patterns displaying rhythms with a frequency that could match the rhythmic operation of many visceral organs. Thus, the meaningful information carried by the sympathetic neural circuits for the visceral controls is likely to be encoded in the dynamics of their spiking patterns. In summary, a dynamic change of neural spiking patterns could be used as a simple scheme for neural information coding.