Responses of neurons in the rostral ventrolateral medulla to whole body rotations: comparisons in decerebrate and conscious cats

Abstract

The responses to vestibular stimulation of brain stem neurons that regulate sympathetic outflow and blood flow have been studied extensively in decerebrate preparations, but not in conscious animals. In the present study, we compared the responses of neurons in the rostral ventrolateral medulla (RVLM), a principal region of the brain stem involved in the regulation of blood pressure, to whole body rotations of conscious and decerebrate cats. In both preparations, RVLM neurons exhibited similar levels of spontaneous activity (median of ∼17 spikes/s). The firing of about half of the RVLM neurons recorded in decerebrate cats was modulated by rotations; these cells were activated by vertical tilts in a variety of directions, with response characteristics suggesting that their labyrinthine inputs originated in otolith organs. The activity of over one-third of RVLM neurons in decerebrate animals was altered by stimulation of baroreceptors; RVLM units with and without baroreceptor signals had similar responses to rotations. In contrast, only 6% of RVLM neurons studied in conscious cats exhibited cardiac-related activity, and the firing of just 1% of the cells was modulated by rotations. These data suggest that the brain stem circuitry mediating vestibulosympathetic reflexes is highly sensitive to changes in body position in space but that the responses to vestibular stimuli of neurons in the pathway are suppressed by higher brain centers in conscious animals. The findings also raise the possibility that autonomic responses to a variety of inputs, including those from the inner ear, could be gated according to behavioral context and attenuated when they are not necessary.

Fig. 1.

A: responses of an rostral ventrolateral medulla (RVLM) neuron to stretch of a carotid artery in a decerebrate cat. Top trace, blood pressure (sampled at 100 Hz); bottom trace, unit activity (sampled at 25,000 Hz). Horizontal line, period during which the artery was stretched. Carotid stretch resulted in a decrease in blood pressure that was preceded by a decline in unit firing. B and C: firing pattern of a RVLM unit with cardiac-related activity recorded in a conscious cat. B and C show results from the same cell. B: averaged changes in carotid blood flow (top) and associated changes in RVLM unit firing (bottom); 169 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. C: raw data for a 1.2-s segment of the run used to generate averages in B. Blood flow was sampled at 100 Hz, and unit activity was sampled at 25,000 Hz. Cardiac-related activity of the unit was not obvious until averaging was performed.

Fig. 2.

Spontaneous firing rates of neurons tested for responses to whole body rotations in decerebrate and conscious animals. Each neuron is represented by ●. Horizontal lines, median firing rates in each preparation.

Fig. 3.

Polar plot showing response vector orientations determined for RVLM neurons in decerebrate cats. Outer ring, data for neurons whose activity was altered by carotid artery stretch (“cardiovascular” neurons). Inner ring, data for neurons that were either not tested for responses to carotid stretch or failed to respond to the stimulus (“not cardiovascular” neurons). Response vector orientations were determined using wobble stimuli, usually at 0.2 Hz (26 of 35 neurons), but at 0.1 Hz for 9 cells and 0.05 Hz for 1 unit. CED, contralateral ear-down roll; IED, ipsilateral ear-down roll; ND, nose-down pitch; NU, nose-up pitch.

Fig. 4.

Averaged responses of a RVLM neuron to sinusoidal rotations of a decerebrate cat. A–D: responses to ear-down (roll) rotations at different frequencies. E: response to pitch (sagittal plane) rotations at 0.2 Hz. Rotation amplitudes were 10° at 0.05–0.1 Hz, 7.5° at 0.2 Hz, and 5° at 0.5 Hz. Numbers of sweeps averaged for each trace are as follows: 3 in A, 4 in B, 10 in C, 27 in D, and 25 in E. Each histogram contains 500 bins (bin width varies from 40 ms at 0.05 Hz to 4 ms at 0.5 Hz). A sine wave superimposed on each trace shows table movement. Response to roll rotations was in phase with table position at low stimulus frequencies but lagged table position slightly at higher frequencies. Response to 0.2-Hz pitch (E) is much smaller than response to 0.2-Hz roll (C), in accordance with response vector orientation calculated using the wobble stimulus (−28°). Contra, contralateral; Ipsi, ipsilateral.

Fig. 5.

Bode plots illustrating responses of RVLM neurons to fixed-plane rotations at multiple frequencies; response gain and phase are plotted in relation to stimulus position. A: individual Bode plots for each cell where responses to rotations were measured at ≥3 frequencies over a stimulus decade (e.g., 0.05–0.5 Hz). To facilitate comparisons, gain at the lowest frequency tested for a neuron (usually 0.05 Hz, but 0.02 Hz for 1 cell and 0.1 Hz for 3 units) was standardized at 1 spike·s⁻¹·degree⁻¹. B: average data for all neurons. Solid lines, average of standardized data in A; dashed lines, unstandardized raw data. Only 1 average is shown for phase, as no standardization occurred.

Fig. 6.

Locations of RVLM neurons whose responses to whole body rotations were examined in decerebrate (A) and conscious (B) animals. Red symbols designate neurons that were activated by cardiovascular (cardio) stimuli; these neurons exhibited cardiac-related firing in conscious animals, or their firing rate was altered by stretch of the carotid artery in decerebrate cats. Large squares, neurons whose firing was modulated by whole body rotations; smaller circles, cells that failed to respond to vestibular stimulation. Numbers below the bottom set of sections indicate the level posterior (P) to stereotaxic zero, in accordance with Berman's atlas (5). 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.