Altered cortical activation patterns associated with baroreflex unloading following 24 h of physical deconditioning

Abstract

Cardiovascular arousal is associated with patterned cortical activity changes. Head-down-tilt bed rest (HDBR) dimishes the baroreflex-mediated cardiac control. The present study tested the hypothesis that HDBR deconditioning would modify the forebrain organization for heart rate (HR) control during baroreflex unloading. Heart rate variability (HRV), blood pressure and plasma hormones were analysed at rest, whereas HR and cortical autonomic activation patterns (functional magnetic resonance imaging) were measured during graded and randomly assigned lower body negative pressure treatments (LBNP, −15 and −35 mmHg) both before (Pre) and after (Post) a 24 h HDBR protocol (study 1; n = 8). An additional group was tested before and following diuretic-induced hypovolaemia (study 2; n = 9; spironolactone, 100 mg day −−1 for 3 days) that mimicked the plasma volume lost during HDBR (−15% in both studies; P < 0.05). Head-down bed rest with hypovolaemia did not affect baseline HR, mean arterial pressure, HRV or plasma catecholamines. Head-down bed rest augmented the LBNP-induced HR response (P < 0.05), and this was associated with bed-rest-induced development of the following changes: (i) enhanced activation within the genual anterior cingulate cortex and the right anterior insular cortex; and (ii) deactivation patterns within the subgenual regions of the anterior cingulate cortex. Diuretic treatment (without HDBR) did not affect baseline HR and mean arterial pressure, but did reduce resting HRV and elevated circulating noradrenaline and plasma renin activity (P < 0.05). The greater HR response to LBNP following diuretic (P < 0.05) was associated with diminished activation of the right anterior insula. Our findings indicate that 24 h of HDBR minimized the impact of diuretic treatment on baseline autonomic and cardiovascular variables. The findings also indicate that despite the similar augmentation of HR responses to LBNP and despite similar pre-intervention cortical activation patterns, HDBR and diuretic treatment produced different effects on the cortical responses, with HDBR affecting anterior cingulate cortex and right insula regions, whereas diuretic treatment affected primarily the right insula alone, but in a direction that was opposite to HDBR. The data indicate that physical deconditioning can induce rapid functional changes within the cortical circuitry associated with baroreflex unloading, changes that are distinct from diuretic-induced hypovolaemia. The results suggest that physical activity patterns exert a rapid and notable impact on the cortical circuitry associated with cardiovascular control.

Efficacy of fluid loading as a countermeasure to the hemodynamic and hormonal changes of 28-h head-down bed rest

“…; Shoemaker et al. ), we found that HDBR resulted in a loss of plasma volume. In contrast to Waters et al.…”

Human cerebral circuitry related to cardiac control: A neuroimaging meta‐analysis

“…The impact of this effect during conditions of evoked HR changes, such as those examined in the current analysis, requires additional study. Moreover, a conceptual difference exists in attempting to understand brain–heart linkages as a specific hypothesis supported strongly by rodent and clinical studies, versus those patterns that can be affected by cardiac patterns.…”

“…Rapid changes in heart rate (HR) or steady state levels of HR variability (HRV) are often interpreted to reflect cardiovagal influences . These markers are able to differentiate neurocardiovascular properties that vary as a function of sex, age, disease, and training state . In the clinical context, a number of individuals express excessive cardiovascular reactions to stress, and such heightened reactivity is predictive of cardiovascular pathology .…”

Forebrain neurocircuitry associated with human reflex cardiovascular control

“…By separating the cortical response to lower levels of lower body suction that emphasize sympathetic activation rather than heart rate changes, these studies emphasized the strong associations between heart rate and increased activation within the right superior insula and the dorsal anterior cingulate during baroreceptor unloading. Of note, these two regions also showed a change in activation pattern following 24 h of head-down tilt bed rest in association with abnormally elevated heart rate responses to −15 mmHg lower body suction (Shoemaker et al, 2012b ) highlighting the consistent observations of this insula-ACC axis in baroreflex-mediated cardiovascular control (Medford and Critchley, 2010 ).…”