Cardiac rhythmicity and burstiness are major characteristics of neuronal firing in medullary autonomic networks across sleep-wake states in freely moving rats

Abstract

Cardiac rhythmicity is a hallmark of the autonomic control system from its sensory inputs all the way to sympathetic efferent nerve discharge directed to the heart and vasculature. Neuron firing in brainstem networks, essential in this control, was studied in great detail under anesthesia but recordings of sympathetic-related neuron firing in freely moving animals remain extremely scarce. We have shown recently [1], that such recordings are possible to perform in freely behaving rats and reported that the pattern of neural activity adheres to the basic principles of organization proposed earlier [2] based on data collected within the constraints of anesthesia, decerebration, or head-restrain. Here we analyzed the firing of sympathetic-related neurons from these recordings over different arousal states. We hypothesized that the essential characteristics, such as rhythmicity and burstiness remain preserved during different sleep-wake states. To address this issue, 23 neurons recorded continuously during waking and sleep in 3 rats were selected. Electrocardiogram, cortical electroencephalogram, and neck muscle electromyogram were recorded along with simultaneous recordings of multiple single neurons using tetrode electrodes or fine wire bundles aimed at central autonomic structures in the medulla as described in [1]. Firing characteristics were analyzed in steady state segments of quiet waking (QW) and slow wave sleep (SWS) as well as during transient events in SWS and REM sleep. We found that steady state discharge of rhythmic bursts was dominant in both QW and SWS even though the average firing rate in the group decreased (from 12.6+1.6 to 7.4+1.3 spike/s) from wake to SWS. Quite remarkably, fluctuations in firing rate within and between QW and SWS were associated with a decrease in the number of bursts rather than the spike per burst ratio. On the other hand, phasic events, such as microarousal associated with transient muscle activity and tachycardia were associated with short (2-5 s) episodes of increase in firing rate characterized by relatively weak cardiac rhythmicity and increased synchronization within the network (i.e. between neurons detected on the same tetrodes).The results show that the study of multiple single neuron relationships in central sympathetic networks is a viable tool to explore autonomic control mechanisms and we emphasize the importance of neural control of cardiovascular adjustments in complex behaviors, including stress, exercise, arousal, sleep-wake states, and different tasks.[1] Kocsis, B.; Topchiy, I., Rhythmic firing of neurons in the medulla of conscious freely behaving rats: rhythmic coupling with baroreceptor input. Pflugers Archiv: Eur J physiol 2022.[2] Barman, S. M., 2019 Ludwig Lecture: Rhythms in sympathetic nerve activity are a key to understanding neural control of the cardiovascular system. Am J Physiol Regul Integr Comp Physiol 2020. NIMH This is the full abstract presented at the American Physiology Summit 2023 meeting and is only available in HTML format. There are no additional versions or additional content available for this abstract. Physiology was not involved in the peer review process.