Laterality Influences Central Integration of Baroreceptor Afferent Input in Male and Female Sprague Dawley Rats.

Ibrahim M Salman,Stephen J Lewis,Omar Z Ameer,Sheridan Mcmurray,Alessandra S Giarola,Arun Sridhar,Yee-Hsee Hsieh

doi:10.3389/fphys.2020.00499

Abstract

We explored the effects of baroreceptor afferents laterality and sexual dimorphism on the expression of cardiovascular reflex responses to baroreflex activation in Sprague Dawley (SD) rats. Under urethane anesthesia, rats of either sex (total n = 18) were instrumented for left, right and bilateral aortic depressor nerve (ADN) stimulation (1–40 Hz, 0.2 ms, 0.4 mA for 20 s) and measurement of mean arterial pressure (MAP), heart rate (HR) and mesenteric (MVR) and femoral (FVR) vascular resistance. Female rats were matched for the diestrus phase of the estrus cycle. Left, right and bilateral ADN stimulation evoked frequency-dependent drops in MAP, HR, and MVR, and increases in FVR. Irrespective of sex, left and bilateral ADN stimulation as compared to right-sided stimulation mediated greater reflex reductions in MAP, HR, and MVR but not in FVR. In males, reflex bradycardic responses were greater in response to bilateral stimulation relative to both left- and right-sided stimulation. In females, left ADN stimulation evoked the largest increase in FVR. Left and bilateral ADN stimulations evoked greater reductions in MAP and MVR while left-sided stimulation produced larger increases in FVR in females compared with males. All other reflex responses to ADN stimulation were relatively comparable between males and females. These results show a differential baroreflex processing of afferent neurotransmission promoted by left versus right baroreceptor afferent inputs and sexual dimorphism in the expression of baroreflex responses in rats of either sex. Collectively, these data add to our understanding of physiological mechanisms pertaining to baroreflex control in both males and females.

Highlights

The arterial baroreceptor reflex is a vital short-term control mechanism that maintains blood pressure (BP) within a relatively narrow range of oscillation (Thomas, 2011; Salman, 2016)
Time-trend profiles illustrating the effect of aortic depressor nerve (ADN) stimulation on recorded cardiovascular parameters (Supplementary Figures S1–S12) and calculated absolute changes in the measured physiological variables (Supplementary Figures S13–S15) are provided in the Online Data Supplement
The principal novel aspects of this study are (1) a superior baroreflex processing of afferent neurotransmission evoked by left aortic baroreceptors, which was primarily evidenced by greater baroreflex-mediated reductions in BP relative to activation of the right afferent fibers in rats of either sex, (2) neurostimulation of baroreceptor afferent input using bilateral ADN stimulation does not offer additive reflex depressor effects and is not superior to left ADN stimulation, (3) in males, but not female, reflex bradycardic responses appear to exhibit an additive pattern when ADN stimulation is delivered bilaterally as opposed to either right or left ADN stimulation, and (4) baroreflex processing of the left or bilateral baroreceptor afferent input in females evokes higher reflex depressor responses compared with males

Summary

Introduction

The arterial baroreceptor reflex is a vital short-term control mechanism that maintains blood pressure (BP) within a relatively narrow range of oscillation (Thomas, 2011; Salman, 2016). An overwhelming number of studies have investigated the role of baroreceptor afferents in the regulation of cardiovascular function and how the afferent neurotransmission is processed centrally in both normal and disease states (Ma et al, 2002; Salman et al, 2014; Salman et al, 2015; Brognara et al, 2016; Kawada et al, 2018). Research in dogs seems to suggest a definite laterality in ADN responses, with data indicating a left-sided dominance in the reflex depressor in response to ADN stimulation (Hasimoto and Hirohata, 1936) and superior baroreflex-mediated changes in arterial pressure with left and bilateral sectioning of baroreceptor afferents relative to the elimination of the right afferent neurons (Walgenbach et al, 1981). On the other hand, such functional evidence is still lacking and, the first objective of our study was to investigate the effect of laterality on the baroreceptor reflex processing of afferent signals in rats and whether measures of cardiovascular reflexes would differ when stimulation of the afferent neurons is delivered on the left side, right side or bilaterally

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Conclusion