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Forebrain neurocircuitry associated with human reflex cardiovascular control.

Shoemaker JK, Goswami R - Front Physiol (2015)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: School of Kinesiology, The University of Western Ontario London, ON, Canada ; Department of Physiology and Pharmacology, The University of Western Ontario London, ON, Canada.

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.

No MeSH data available.


Related in: MedlinePlus

Meta-analysis summary of data from our laboratory (n = 124) (Wong et al., 2007a,b; Al-Otaibi et al., 2010; Goswami et al., 2011; Norton et al., 2013) of common cortical regions associated with heart rate control during non-fatiguing handgrip exercise task [this figure originally published in Shoemaker et al. (2015) (used with permission)]. These participants each performed 3–7 bouts of moderate intensity (35–40% maximal strength) handgrip tasks each lasting 30 s. Left panels with red dots: Cortical areas of increased activation relative to baseline in response to short duration, moderate intensity isometric handgrip exercise. Right panels with blue dots: Cortical areas of decreased activation relative to baseline in response to short duration, moderate intensity isometric handgrip exercise. FDR pN = 0.01; Min Volume (mm3) = 200. Analysis performed using GingerALE (Version 2.3.2; BrainMap) and Mango (Version 3.1.2; Research Imaging Institute, University of Texas Health Science Center) (Eickhoff et al., 2011; Turkeltaub et al., 2012). MPFC, medial prefrontal cortex; IC, insula cortex; dACC, dorsal anterior cingulate cortex; PCC, posterior cingulate cortex; MC, motor cortex; SC, sensory cortex; TH, thalamus; HC, hippocampus. Images are in radiological presentation with right side of the brain (R) on left, and left side of the brain (L) on the right. A, anterior; P, posterior.
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Figure 1: Meta-analysis summary of data from our laboratory (n = 124) (Wong et al., 2007a,b; Al-Otaibi et al., 2010; Goswami et al., 2011; Norton et al., 2013) of common cortical regions associated with heart rate control during non-fatiguing handgrip exercise task [this figure originally published in Shoemaker et al. (2015) (used with permission)]. These participants each performed 3–7 bouts of moderate intensity (35–40% maximal strength) handgrip tasks each lasting 30 s. Left panels with red dots: Cortical areas of increased activation relative to baseline in response to short duration, moderate intensity isometric handgrip exercise. Right panels with blue dots: Cortical areas of decreased activation relative to baseline in response to short duration, moderate intensity isometric handgrip exercise. FDR pN = 0.01; Min Volume (mm3) = 200. Analysis performed using GingerALE (Version 2.3.2; BrainMap) and Mango (Version 3.1.2; Research Imaging Institute, University of Texas Health Science Center) (Eickhoff et al., 2011; Turkeltaub et al., 2012). MPFC, medial prefrontal cortex; IC, insula cortex; dACC, dorsal anterior cingulate cortex; PCC, posterior cingulate cortex; MC, motor cortex; SC, sensory cortex; TH, thalamus; HC, hippocampus. Images are in radiological presentation with right side of the brain (R) on left, and left side of the brain (L) on the right. A, anterior; P, posterior.

Mentions: The effects of general anaesthesia on autonomic function, along with limitations in the number of sites that can be examined simultaneously, represent challenges in interpreting cortical function from an experimental rodent model. Thus, an important experimental goal has been to establish the translational success of the rodent models back into the conscious human model. Two paradigms have been used to accomplish this goal. First, electrical stimulation of brain regions in awake epileptic patients with indwelling electrodes have been performed in a very limited extent and, when performed, still only expose one site at a time. Nonetheless, this model has reinforced the important role that focal regions of the IC have (or do not have) on cardiac function (Oppenheimer et al., 1992a; Al-Otaibi et al., 2010), the details of which are outlined below. More recently, the introduction of functional magnetic resonance imaging (fMRI) (Ogawa et al., 1990, 1992) has enabled studies of the temporal and spatial patterns of cortical activation patterns in conscious humans. The first fMRI report to study reflex cardiovascular control in humans (King et al., 1999) outlined a large group of forebrain regions co-activated during maximal effort maneuvers such as a Valsalva maneuver or maximal handgrip effort. Subsequently, numerous studies have begun to detail the cortical autonomic network in conscious humans, the networked nature of these sites, and their potential role in cardiovascular control. A meta-analysis of exercise-specific outcomes from our laboratory (Shoemaker et al., 2015) suggests an important role of the MPFC, IC, dorsal ACC and hippocampus (see Figure 1). However, this pattern may be specific to volitional exercise. In fact, a recent study used activation likelihood estimation meta-analysis of a number of human neuroimaging experiments and identified a set of consistently activated brain regions, comprising left amygdala, right anterior and left posterior IC and midcingulate cortices that form the core of the central autonomic network (Beissner et al., 2013). Thus, overall, a distinct group of forebrain and midbrain regions are now understood to be involved in cardiovascular control and these regions may vary from reflex to reflex.


Forebrain neurocircuitry associated with human reflex cardiovascular control.

Shoemaker JK, Goswami R - Front Physiol (2015)

Meta-analysis summary of data from our laboratory (n = 124) (Wong et al., 2007a,b; Al-Otaibi et al., 2010; Goswami et al., 2011; Norton et al., 2013) of common cortical regions associated with heart rate control during non-fatiguing handgrip exercise task [this figure originally published in Shoemaker et al. (2015) (used with permission)]. These participants each performed 3–7 bouts of moderate intensity (35–40% maximal strength) handgrip tasks each lasting 30 s. Left panels with red dots: Cortical areas of increased activation relative to baseline in response to short duration, moderate intensity isometric handgrip exercise. Right panels with blue dots: Cortical areas of decreased activation relative to baseline in response to short duration, moderate intensity isometric handgrip exercise. FDR pN = 0.01; Min Volume (mm3) = 200. Analysis performed using GingerALE (Version 2.3.2; BrainMap) and Mango (Version 3.1.2; Research Imaging Institute, University of Texas Health Science Center) (Eickhoff et al., 2011; Turkeltaub et al., 2012). MPFC, medial prefrontal cortex; IC, insula cortex; dACC, dorsal anterior cingulate cortex; PCC, posterior cingulate cortex; MC, motor cortex; SC, sensory cortex; TH, thalamus; HC, hippocampus. Images are in radiological presentation with right side of the brain (R) on left, and left side of the brain (L) on the right. A, anterior; P, posterior.
© Copyright Policy
Related In: Results  -  Collection

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Figure 1: Meta-analysis summary of data from our laboratory (n = 124) (Wong et al., 2007a,b; Al-Otaibi et al., 2010; Goswami et al., 2011; Norton et al., 2013) of common cortical regions associated with heart rate control during non-fatiguing handgrip exercise task [this figure originally published in Shoemaker et al. (2015) (used with permission)]. These participants each performed 3–7 bouts of moderate intensity (35–40% maximal strength) handgrip tasks each lasting 30 s. Left panels with red dots: Cortical areas of increased activation relative to baseline in response to short duration, moderate intensity isometric handgrip exercise. Right panels with blue dots: Cortical areas of decreased activation relative to baseline in response to short duration, moderate intensity isometric handgrip exercise. FDR pN = 0.01; Min Volume (mm3) = 200. Analysis performed using GingerALE (Version 2.3.2; BrainMap) and Mango (Version 3.1.2; Research Imaging Institute, University of Texas Health Science Center) (Eickhoff et al., 2011; Turkeltaub et al., 2012). MPFC, medial prefrontal cortex; IC, insula cortex; dACC, dorsal anterior cingulate cortex; PCC, posterior cingulate cortex; MC, motor cortex; SC, sensory cortex; TH, thalamus; HC, hippocampus. Images are in radiological presentation with right side of the brain (R) on left, and left side of the brain (L) on the right. A, anterior; P, posterior.
Mentions: The effects of general anaesthesia on autonomic function, along with limitations in the number of sites that can be examined simultaneously, represent challenges in interpreting cortical function from an experimental rodent model. Thus, an important experimental goal has been to establish the translational success of the rodent models back into the conscious human model. Two paradigms have been used to accomplish this goal. First, electrical stimulation of brain regions in awake epileptic patients with indwelling electrodes have been performed in a very limited extent and, when performed, still only expose one site at a time. Nonetheless, this model has reinforced the important role that focal regions of the IC have (or do not have) on cardiac function (Oppenheimer et al., 1992a; Al-Otaibi et al., 2010), the details of which are outlined below. More recently, the introduction of functional magnetic resonance imaging (fMRI) (Ogawa et al., 1990, 1992) has enabled studies of the temporal and spatial patterns of cortical activation patterns in conscious humans. The first fMRI report to study reflex cardiovascular control in humans (King et al., 1999) outlined a large group of forebrain regions co-activated during maximal effort maneuvers such as a Valsalva maneuver or maximal handgrip effort. Subsequently, numerous studies have begun to detail the cortical autonomic network in conscious humans, the networked nature of these sites, and their potential role in cardiovascular control. A meta-analysis of exercise-specific outcomes from our laboratory (Shoemaker et al., 2015) suggests an important role of the MPFC, IC, dorsal ACC and hippocampus (see Figure 1). However, this pattern may be specific to volitional exercise. In fact, a recent study used activation likelihood estimation meta-analysis of a number of human neuroimaging experiments and identified a set of consistently activated brain regions, comprising left amygdala, right anterior and left posterior IC and midcingulate cortices that form the core of the central autonomic network (Beissner et al., 2013). Thus, overall, a distinct group of forebrain and midbrain regions are now understood to be involved in cardiovascular control and these regions may vary from reflex to reflex.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: School of Kinesiology, The University of Western Ontario London, ON, Canada ; Department of Physiology and Pharmacology, The University of Western Ontario London, ON, Canada.

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.

No MeSH data available.


Related in: MedlinePlus