The response of the vestibulosympathetic reflex to linear acceleration in the rat

Abstract

The vestibulosympathetic reflex (VSR) increases blood pressure (BP) upon arising to maintain blood flow to the brain. The optimal directions of VSR activation and whether changes in heart rate (HR) are associated with changes in BP are still not clear. We used manually activated pulses and oscillatory linear accelerations of 0.2-2.5 g along the naso-occipital, interaural, and dorsoventral axes in isoflurane-anesthetized, male Long-Evans rats. BP and HR were recorded with an intra-aortic sensor and acceleration with a three-dimensional accelerometer. Linear regressions of BP changes in accelerations along the upward, downward, and forward axes had slopes of ≈3-6 mmHg · g-1 (P < 0.05). Lateral and backward accelerations did not produce consistent changes in BP. Thus upward, downward, and forward translations were the directions that significantly altered BP. HR was unaffected by these translations. The VSR sensitivity to oscillatory forward-backward translations was ≈6-10 mmHg · g-1 at frequencies of ≈0.1 Hz (0.2 g), decreasing to zero at frequencies above 2 Hz (1.8 g). Upward, 70° tilts of an alert rat increased BP by 9 mmHg · g-1 without changes in HR, indicating that anesthesia had not reduced the VSR sensitivity. The similarity in BP induced in alert and anesthetized rats indicates that the VSR is relatively insensitive to levels of alertness and that the VSR is likely to cause changes in BP through modification of peripheral vascular resistance. Thus the VSR, which is directed toward the cardiovascular system, is in contrast to the responses in the alert state that can produce sweating, alterations in BP and HR, and motion sickness.

Keywords: anesthesia; blood pressure; heart rate; linear acceleration; translation.

Copyright © 2016 the American Physiological Society.

Figures

Fig. 1.

Coordinate system used in this study. The positive direction of head translation along the x-axis was forward, along the y-axis was leftward, and along the z-axis was upward. The rat's body was prone during these experiments.

Fig. 2.

Changes in blood pressure (BP) and heart rate (HR) during breathing cycle in the tested rats. A: example of BP recorded with an intra-aortic sensor and breathing (Br) rate with a balloon placed under the rat's belly. The data were processed to extract systolic BP (Sys BP) and HR. The pressure in the balloon increased during inspiration and decreased during expiration to indicate breathing rate. Each inspiration peak is marked by a vertical, dashed line (Inspiration). There was tight synchronization of inspiration with minimal values of systolic BP. There was no relationship of HR changes to breathing cycle. B–I: example of average systolic BP and HR changes during breathing cycle in each rat tested in this study. Approximately 100 intervals were synchronized by minimal systolic BP (Inspiration) and averaged. Black lines are average values; gray lines are individual values of the breathing ranges. Data are shown over 1.5 s before and after minimal systolic BP. Arrows point to inspiration peaks (Inspiration).

Fig. 3.

A–E: increases in systolic BP (bottom traces) in response to upward (+z) accelerations (top traces). Each increase in upward acceleration caused an associated increase in BP. Each set of traces is from a different rat. Note the regularity of the stimulus pulses and of the BP responses. F–J: decreases in BP (bottom traces) in response to downward (−z) accelerations. Downward accelerations also reliably evoked reductions in BP. The small drops in BP at the onset of the accelerations were due to inspiration. Approximately 20 traces are superimposed in each of the traces in A–J. K and L: averaged responses from A–J. There was an increase in BP associated with the upward acceleration in each rat (K) and a decrease in BP with downward acceleration in each animal associated with the downward acceleration (L). Only 1 animal had changes in HR associated with the upward acceleration (K). No changes in HR were observed in association with downward acceleration. Time in seconds on abscissa; BP in millimeters of mercury on the ordinate.

Fig. 4.

Changes in BP in response to forward (A–E) and backward (F–J) translation. Top traces: positive (A–E) and negative (F–J) x-axis linear accelerations; 20 trials in each. Bottom traces: BP. Forward (+x) acceleration generally produced increases in BP, whereas the backward (−x) accelerations did not cause regular changes in BP. K and L: averaged accelerations demonstrate that there were regular increases in BP when moving forward along the x-axis (K) but not when moving backward along the −x-axis (L). No changes in HR were observed in association with forward or backward accelerations. Time in seconds on abscissa; BP in millimeters of mercury on the ordinate.

Fig. 5.

Changes in BP during lateral (+y- and −y-axis) translation. Top traces: linear accelerations; bottom traces: BP. A–E: left (+y) axis translation; F–J: right (−y) axis translation. Twenty responses overlaid in each stimulus sequence. There were intermittent responses that were not synchronized with the stimuli. K and L: averaged responses for each of the 5 rats. There were increases (K) and decreases (L) in some rats, but they were not well synchronized with the linear accelerations. Time in seconds on abscissa; BP in millimeters of mercury on the ordinate.

Fig. 6.

Changes in BP induced by translation at 1 g along x- and z-axes in rats R004 (A), R006 (B), R009 (C), R010 (D), and R011 (E). The arrows point to the average responses for individual rats (see Table 2). Black arrows point to responses induced by upward and forward translations; gray arrows point to responses induced by downward and backward translations.

Fig. 7.

Scatter plots of changes in systolic BP as a function of peak linear acceleration in a (typical) rat. Each dot represents a single trial. Plots show results of upward (A), downward (B), forward (C), backward (D), leftward (E), and rightward (F) acceleration. The confidence levels of the linear regressions are shown below each graph. A–C: the linear regressions through the data had a significant correlation for 3 of the data sets [upward (A), downward (B), and forward (C)]. Despite the intermittent changes in BP when the animal was translated back (D), left (E), and right (F), the magnitude of the responses did not correlate with the magnitude of acceleration. Abscissa, magnitude of acceleration; ordinate, change in BP in millimeters of mercury.

Fig. 8.

Effects of frequency of oscillation on activation of BP. A–E: changes in BP in response to linear oscillation at sinusoidal translation about the x-axis at ≈0.3 Hz (0.4 g). A: systolic and diastolic BP; B: systolic BP, fit with a sinusoid; C: sinusoidal changes in HR; D: the activating stimulus, i.e., the linear accelerations at ±0.4 g along the x-axis; E: lateral acceleration during the sinusoidal activation in D. F and G: the sensitivity (F) and phase (G) of the VSR induced by translation along the x-axis (forward, backward) as a function of stimulus frequency (abscissa). The 0 phases corresponded to forward motion. Note that the peak modulations were maximal at frequencies <1 cycle/s (G) and that the phases were 0 at these frequencies. H and I: there was no correlation with changes in BP when the oscillations were in the lateral (±y) direction (H), and the phases were widely distributed (I). Gray, horizontal bars in F and G are breathing-frequency range of this rat (average ± 1 SD).

Fig. 9.

The sensitivities (A and C) and the phases (B and D) of the VSR as a function of stimulus frequencies (abscissa) for the other 4 animals in this series. The animals were oscillated at different frequencies along the ±x-axis (forward-back; A and B) and the ±y-axis (side-to-side; C and D) by sinusoidal translation along the x-axis. The 0 phase corresponded to forward (B) and leftward (D) accelerations. In each rat, the sensitivities were maximal at oscillation frequencies below 1 Hz, and the phases were 0, i.e., in the forward direction. There was no similar relationship during ±y-axis oscillation (C and D). Gray, horizontal bars in A and B are breathing-frequency range of this rat (average ± 1 SD).