Forebrain neurocircuitry associated with human reflex cardiovascular control

Abstract

Physiological homeostasis depends upon adequate integration and responsiveness of sensory information with the autonomic nervous system to affect rapid and effective adjustments in end organ control. Dysregulation of the autonomic nervous system leads to cardiovascular disability with consequences as severe as sudden death. The neural pathways involved in reflexive autonomic control are dependent upon brainstem nuclei but these receive modulatory inputs from higher centers in the midbrain and cortex. Neuroimaging technologies have allowed closer study of the cortical circuitry related to autonomic cardiovascular adjustments to many stressors in awake humans and have exposed many forebrain sites that associate strongly with cardiovascular arousal during stress including the medial prefrontal cortex, insula cortex, anterior cingulate, amygdala and hippocampus. Using a comparative approach, this review will consider the cortical autonomic circuitry in rodents and primates with a major emphasis on more recent neuroimaging studies in awake humans. A challenge with neuroimaging studies is their interpretation in view of multiple sensory, perceptual, emotive and/or reflexive components of autonomic responses. This review will focus on those responses related to non-volitional baroreflex control of blood pressure and also on the coordinated responses to non-fatiguing, non-painful volitional exercise with particular emphasis on the medial prefrontal cortex and the insula cortex.

Cardiovascular and autonomic reactivity to psychological stress: Neurophysiological substrates and links to cardiovascular disease

“…Specifically, forebrain areas can functionally interact with one another as a network to modulate visceromotor and viscerosensory functions of cell groups within the thalamus, hypothalamus, PAG and medullary regions – which govern and monitor autonomic and neuroendocrine outflow to the heart and blood vessels in coordination with behavioral actions and motivated dispositions to act (Bandler, Keay, Floyd, & Price, 2000; Öngür & Price, 2000; Saper, 2002; Ulrich-Lai & Herman, 2009). Across several recent brain-imaging studies, stressor-evoked cardiovascular changes (e.g., in BP and HR) have been reliably associated with activity changes in these forebrain and subcortical regions, consistent with invasive animal work and patient lesion studies on central cardiovascular, autonomic, and neuroendocrine control (Critchely et al, 2003; Oppenheimer & Cechetto, 2016; Shoemaker et al, 2015; Shoemaker & Goswami, 2015). Conventionally, these forebrain and subcortical regions have been referred to as components or nodes of a central autonomic network (Bennarroch, 1993; Saper, 2002) or, more inclusively, a visceral control network.…”

“…As detailed in recent meta-analyses and other reviews (e.g., Gianaros & Wager, 2015; Thayer et al, 2012; Myers 2016; Shoemaker & Goswami, 2015; Beissner et al 2013, Muscatell & Eisenberger), functional divisions of the anterior cingulate cortex (ACC) and adjacent medial prefrontal cortex (mPFC), insula, hippocampus, and amygdala may be viewed as a core – albeit not exclusive – components of a broader network of forebrain systems involved in mediating stressor-evoked changes in cardiovascular activity. These forebrain systems are specifically viewed to play a role in stress appraisal processes, by ascribing personal and threat-related meaning to events, contexts, and other sources of information that are encoded and experienced (Gianaros & Wager, 2015).…”

“…And, over what time scale? In these regards, methodological advances in brain-imaging and concurrent physiological monitoring have not yet enabled researchers to readily differentiate the neural correlates of afferent and efferent processes in the context of stressor-evoked cardiovascular reactions, as has been done with other physiological adjustments (e.g., with exercise or baroreceptor unloading ; Shoemaker & Goswami, 2015; Shoemaker et al, 2015; Shoemaker, Wong, & Cechetto, 2012). Another major frontier for future work on stressor-evoked cardiovascular reactivity will be to integrate emerging image acquisition methods for more precise functional assessments of brainstem circuits, which relay both descending stressor-evoked visceromotor commands from forebrain areas and ascending viscerosensory information from the periphery to these forebrain areas (Beissner, 2015; Beissner et al, 2014; Bar et al, 2016).…”

Brain Regional Blood Flow and Working Memory Performance Predict Change in Blood Pressure Over 2 Years

“…Overall, frontostriatal areas showed a suppression of rCBF during task performance, but individuals with greater progression of SBP showed increased frontostriatal rCBF during the tasks. Frontostriatal areas are known to have both excitatory and inhibitory influences on limbic areas inducing sympathetic activation with cortical inhibitory effects on excitatory striatum effects more commonly observed 31 . Insular-subcortical activation was significantly and positively related to frontostriatal activation in the current data.…”

Bidirectional asymmetry in the neurovisceral communication for the cardiovascular control: New insights

“…Th e prefrontal cortex and subcortical areas such as the amygdala form a reciprocal inhibitory circuit (Shoemaker and Goswami 2015), the function of which is to regulate the behavioral and emotional responses to adapt the body to environmental demands and control the function of the ANS aff ecting the heart and other organs (Williams et al 2015). Th ese authors have suggested that this circuit could serve as a connection (mediated by the ANS) between the emotional and physiological processes and that its level of activity could be monitored by the HRV.…”