Brain systems for baroreflex suppression during stress in humans

Abstract

The arterial baroreflex is a key mechanism for the homeostatic control of blood pressure (BP). In animals and humans, psychological stressors suppress the capacity of the arterial baroreflex to control short-term fluctuations in BP, reflected by reduced baroreflex sensitivity (BRS). While animal studies have characterized the brain systems that link stressor processing to BRS suppression, comparable human studies are lacking. Here, we measured beat-to-beat BP and heart rate (HR) in 97 adults who performed a multisource interference task that evoked changes in spontaneous BRS, which were quantified by a validated sequence method. The same 97 participants also performed the task during functional magnetic resonance imaging (fMRI) of brain activity. Across participants, task performance (i) increased BP and HR and (ii) reduced BRS. Analyses of fMRI data further demonstrated that a greater task-evoked reduction in BRS covaried with greater activity in brain systems important for central autonomic and cardiovascular control, particularly the cingulate cortex, insula, amygdala, and midbrain periaqueductal gray (PAG). Moreover, task performance increased the functional connectivity of a discrete area of the anterior insula with both the cingulate cortex and amygdala. In parallel, this same insula area showed increased task-evoked functional connectivity with midbrain PAG and pons. These novel findings provide human evidence for the brain systems presumptively involved in suppressing baroreflex functionality, with relevance for understanding the neurobiological mechanisms of stressor-related cardiovascular reactivity and associated risk for essential hypertension and atherosclerotic heart disease.

A Brain Phenotype for Stressor‐Evoked Blood Pressure Reactivity

“…Psychological stressors may also affect other parameters of the baroreflex, including resetting effects on sympathetic vasomotor control over a higher operating range of BP,1 but such effects have been less well studied in humans. Notably, it has been reported that individuals who exhibit greater stressor‐evoked activation in forebrain, midbrain, and brainstem systems for autonomic and visceral control also exhibit a greater stressor‐evoked reduction in cardiovagal baroreflex sensitivity 55. Moreover, several of the areas previously reported to associate with stressor‐evoked reductions in baroreflex sensitivity overlap with those that were predictive of stressor‐evoked BP reactivity within the multivariate pattern (illustrated in Figure 4), including the dorsal and perigenual areas of the anterior cingulate cortex, ventromedial prefrontal cortex, and insula.…”

Where Pain Meets Action in the Human Brain

“…It is likely that the insula integrates nociceptive information into subjective terms (Craig, 2003;Paulus, 2007), and AI is involved in classifying and anticipating painful stimuli (Wiech et al, 2010). The bilateral insula clusters seen in the ALE meta-analysis may thus reflect pain-related signaling either not closely coupled with voluntary action or more closely coupled with another type of efferent response, such as autonomic regulation (Critchley et al, 2004;Gianaros et al, 2012).…”

Effect of Parasympathetic Stimulation on Brain Activity During Appraisal of Fearful Expressions

“…Outputs from the amygdala innervate hypothalamic and brainstem autonomic circuits to trigger autonomic arousal responses to emotional challenges, particularly threats (LeDoux, 2000). Amygdalainduced autonomic arousal is expressed as increased sympathetic activity and/or decreased HRV (Critchley et al, 2005b;Gianaros et al, 2012). The amygdala is also sensitive to feedback from the periphery regarding state of bodily arousal (Critchley et al, 2002).…”