Vagus nerve spiking activity associated with locomotion and cortical arousal states in a freely moving rat

Abstract

The vagus nerve serves as a central pathway for communication between the central and peripheral organs. Despite traditional knowledge of vagus nerve functions, detailed neurophysiological dynamics of the vagus nerve in naïve behavior remain to be understood. In this study, we developed a new method to record spiking patterns from the cervical vagus nerve while simultaneously monitoring central and peripheral organ bioelectrical signals in a freely moving rat. When the rats transiently elevated locomotor activity, the frequency of vagus nerve spikes was correspondingly increased, and this activity was retained for several seconds after the increase in running speed terminated. Spike patterns of the vagus nerve were not robustly associated with which arms the animals entered on an elevated plus maze. During sniffing behavior, vagus nerve spikes were nearly absent. During stopping, the vagus nerve spike patterns differed considerably depending on external contexts and peripheral activity states associated with cortical arousal levels. Stimulation of the vagus nerve altered rat's running speed and cortical arousal states depending on running speed at the instant of stimulation. These observations are a new step for uncovering the physiological dynamics of the vagus nerve modulating the visceral organs such as cardiovascular, respiratory, and gastrointestinal systems.

Multi-channel intraneural vagus nerve recordings with a novel high-density carbon fiber microelectrode array

“…Although electrical stimulation-evoked responses can be useful in determining the type of activated fibers, these responses do not represent physiological neural signaling. A few research groups have obtained physiological neural recordings from autonomic nerves using extraneural cuff electrodes [31][32][33][34][35] . However, extraneural electrodes lack spatial selectivity, as these electrodes record the compound activity of hundreds to thousands of axons from outside the nerve.…”

Sniffing behaviour‐related changes in cardiac and cortical activity in rats

“…Using a new recording method that can monitor the spike pattern of the VN fibres by means of a cuff‐shaped electrode, we revealed that the frequency of VN spikes was higher in novel conditions than in familiar conditions (Shikano et al . ). In addition to this finding, this study showed that there were no prominent differences in the frequency of VN spikes between HF sniffing and RR.…”

“…For VN signals, a spike unit was detected when the amplitude of a negative deflection of the extracellularly recorded signals exceeded a threshold of 7-20 µV, which corresponded to five standard deviations from the baseline of the VN signals recorded during quiescent periods in individual animals. Burst spike units detected within a 10 ms bin were regarded as a single spike (Shikano et al 2019).…”

“…For all steps of an incision, the skin at the incision site was sterilized with betadine and 70% ethanol. For each rat, an incision was made on the left side of the neck from the larynx to the sternum, and the left cervical VN was enclosed in a custom-made cuff-shaped VN electrode (Unique Medical Co. Ltd, Japan; inner diameter, 0.5-1.0 mm; electrode area, 0.25 mm 2 ; cathode-anode interval, 1.5-2.0 mm; and total length, 4.0 mm; for more details, see Shikano et al 2019). All rats then underwent surgery to implant the ECG, EMG and LFP electrodes.…”

“…To this end, we performed simultaneous recordings of local field potential (LFP) signals from the motor cortex and the olfactory bulb (OB), an electrocardiogram (ECG) signal, a dorsal neck muscle electromyogram (EMG) signal, and a VN electrophysiological signal from freely moving rats using our recording technique (Okada et al 2016;Sasaki et al 2017;Shikano et al 2018Shikano et al , 2019. Conventionally, the sniff frequency of rodents is quantified based on respiration-locked intranasal pressure or the temperature of nasal air flow (Clarke et al 1970;Cheung et al 2009).…”