Rhythmic activity of neurons in the rostral ventrolateral medulla of conscious cats: effect of removal of vestibular inputs

Abstract

Although it is well established that bulbospinal neurons located in the rostral ventrolateral medulla (RVLM) play a pivotal role in regulating sympathetic nerve activity and blood pressure, virtually all neurophysiological studies of this region have been conducted in anesthetized or decerebrate animals. In the present study, we used time- and frequency-domain analyses to characterize the naturally occurring discharges of RVLM neurons in conscious cats. Specifically, we compared their activity to fluctuations in carotid artery blood flow to identify neurons with cardiac-related (CR) activity; we then considered whether neurons with CR activity also had a higher-frequency rhythmic firing pattern. In addition, we ascertained whether the surgical removal of vestibular inputs altered the rhythmic discharge properties of RVLM neurons. Less than 10% of RVLM neurons expressed CR activity, although the likelihood of observing a neuron with CR activity in the RVLM varied between recording sessions, even when tracking occurred in a very limited area and was higher after vestibular inputs were surgically removed. Either a 10-Hz or a 20- to 30-Hz rhythmic discharge pattern coexisted with the CR discharges in some of the RVLM neurons. Additionally, the firing rate of RVLM neurons, including those with CR activity, decreased after vestibular lesions. These findings raise the prospect that RVLM neurons may or may not express rhythmic firing patterns at a particular time due to a variety of influences, including descending projections from higher brain centers and sensory inputs, such as those from the vestibular system.

Fig. 1.

A: one-second sample of spontaneous neural activity recorded from the rostral ventrolateral medulla (RVLM) (bottom) and simultaneously recorded CBF (top). Red and blue arrows in the bottom panel respectively designate the two units that could be distinguished using spike detection and sorting software. Carotid artery blood flow (CBF) was sampled at 100 Hz, and unit activity was sampled at 25,000 Hz. B: average action potential waveforms for the two units distinguished using spike sorting. The action potential indicated in red represents the average of 1,613 waveforms sampled during a 132-s period, whereas the action potential indicated in blue represents 4,062 waveforms. The two waveforms were distinct and could be segregated easily. C: averaged changes in CBF (bottom) and associated changes in the activity of the unit designated by blue arrows in A (top); 170 sweeps were pooled to generate traces. Averaging was triggered by maximal carotid blood flow at the central peak. The neuron had its highest probability of firing after each blood flow peak, as flow through the carotid artery was declining. The unit designated by red arrows in A lacked such powerful cardiac-related (CR) activity.

Fig. 2.

Coexistence of CR and 10-Hz activity in an RVLM neuron in a vestibular-intact, conscious cat. A: traces (top to bottom), carotid blood flow (CBF)-triggered average of the CBF signal and CBF-triggered histograms of intervals between consecutive cycles of CBF (CBF Peak-to-Peak Int.) and of RVLM neuronal activity (Pk CBF-to-Unit Int.). Traces were triggered by an event coinciding with the peak of the CBF signal and are based on 426 trials (10-ms bin resolution). In the Pk CBF-to-Unit Int, the asterisks mark the bins used to calculate “peak counts”, and the horizontal line through the histogram is at “background counts”. B: interspike interval histogram (ISIH) of RVLM neuronal activity (Unit-to-Unit Int.; 3-ms bin resolution). C: frequency-domain analyses showing (top to bottom) autospectra of CBF (CBF AS) and RVLM neuronal activity (Unit AS) and the corresponding coherence function relating neuronal activity to the CBF signal (CBF-Unit Coh). Spectra are based on 34 5-s windows; frequency resolution is 0.2 Hz per bin.

Fig. 3.

Coexistence of cardiac-related (CR) and 20- to 30-Hz activity in an RVLM neuron in a conscious cat after labyrinthectomy. The order of the traces is the same as in Fig. 2. A: CBF-triggered analysis is based on 360 trials (10-ms bin resolution). B: ISIH of RVLM neuronal activity (3-ms bin resolution). C: spectra are based on 28 5-s windows; frequency resolution is 0.2 Hz per bin.

Fig. 4.

A: locations of RVLM neurons with CR activity. Black symbols designate neurons whose activity was recorded when vestibular inputs were present (prelesion), whereas red symbols indicate neurons examined following peripheral vestibular lesions (postlesion). Squares denote neurons with combined CR activity and higher-frequency rhythmic discharges (10 Hz or 20–30 Hz); circles denote neurons with CR activity but no evident higher-frequency rhythmic discharges. Numbers above each section indicate the level posterior (P) to stereotaxic zero, in accordance with Berman's atlas (12). 5SP, spinal trigeminal nucleus; 5ST, spinal trigeminal tract; 12N, hypoglossal nerve; CD, dorsal cochlear nucleus; CI, inferior central nucleus; CX, external cuneate nucleus; IO, inferior olive; P, pyramid; PH, nucleus prepositus hypoglossi; PPR, postpyramidal nucleus of the raphe; RB, restiform body; SA, stria acustica; VIN, inferior vestibular nucleus; VMN, medial vestibular nucleus. B: coordinates of each recording site, based on histological reconstructions, with respect to stereotaxic zero (AP), the midline (ML), and the ventral surface of the brain stem (Depth). Black or gray symbols designate neurons whose activity was recorded prior to lesions, whereas red symbols indicate neurons sampled following lesions. Small squares indicate cells without CR activity, whereas larger circles indicate cells with CR firing patterns.

Fig. 5.

Percentage of RVLM neurons sampled on each recording day with cardiac-related activity (CR neurons). Solid squares (■) designate data recorded prior to removal of vestibular inputs (prelesion), whereas open circles (○) indicate findings in animals with peripheral lesions of the vestibular system (postlesion). For days where no symbols are provided, either no data collection occurred or sampling was performed outside of the RVLM. The fraction of RVLM neurons with CR activity varied tremendously from day to day, from 0% to 60% of the sampled population.

Fig. 6.

A: percentage of RVLM neurons with CR activity recorded on each day, prior (prelesion) and subsequent (postlesion) to the surgical elimination of vestibular inputs. Long horizontal bars designate the median percentage of neurons sampled daily with CR activity. B: average spontaneous firing rates for RVLM neurons with and without CR activity. Solid bars designate prelesion firing rates, while open bars indicate postlesion firing rates. Error bars designate one standard error.