Brain correlates of autonomic modulation: Combining heart rate variability with fMRI

MGH/MIT/HMS Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02119, USA.
NeuroImage (Impact Factor: 6.36). 08/2008; 42(1):169-77. DOI: 10.1016/j.neuroimage.2008.04.238
Source: PubMed


The central autonomic network (CAN) has been described in animal models but has been difficult to elucidate in humans. Potential confounds include physiological noise artifacts affecting brainstem neuroimaging data, and difficulty in deriving non-invasive continuous assessments of autonomic modulation. We have developed and implemented a new method which relates cardiac-gated fMRI timeseries with continuous-time heart rate variability (HRV) to estimate central autonomic processing. As many autonomic structures of interest are in brain regions strongly affected by cardiogenic pulsatility, we chose to cardiac-gate our fMRI acquisition to increase sensitivity. Cardiac-gating introduces T1-variability, which was corrected by transforming fMRI data to a fixed TR using a previously published method [Guimaraes, A.R., Melcher, J.R., et al., 1998. Imaging subcortical auditory activity in humans. Hum. Brain Mapp. 6(1), 33-41]. The electrocardiogram was analyzed with a novel point process adaptive-filter algorithm for computation of the high-frequency (HF) index, reflecting the time-varying dynamics of efferent cardiovagal modulation. Central command of cardiovagal outflow was inferred by using the resample HF timeseries as a regressor to the fMRI data. A grip task was used to perturb the autonomic nervous system. Our combined HRV-fMRI approach demonstrated HF correlation with fMRI activity in the hypothalamus, cerebellum, parabrachial nucleus/locus ceruleus, periaqueductal gray, amygdala, hippocampus, thalamus, and dorsomedial/dorsolateral prefrontal, posterior insular, and middle temporal cortices. While some regions consistent with central cardiovagal control in animal models gave corroborative evidence for our methodology, other mostly higher cortical or limbic-related brain regions may be unique to humans. Our approach should be optimized and applied to study the human brain correlates of autonomic modulation for various stimuli in both physiological and pathological states.

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    • "These regions were also reported to be activated by the nociceptive responses to heat, capsaicin, or mechanical stimulation applied to the hand or forearm skin by using positron emission tomography and fMRI (Peyron et al., 2000). However, the supplementary motor area and cerebellum were known to be involved in the regulation of sympathetic activity (Beissner et al., 2013), as revealed by significant correlations between fMRI signal and instantaneous high frequency power of heart rate changes (Napadow et al., 2008). "
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    ABSTRACT: In a human fMRI study, it has been demonstrated that tasting and ingesting capsaicin activate the ventral part of the middle and posterior short gyri (M/PSG) of the insula which is known as the primary gustatory area, suggesting that capsaicin is recognized as a taste. Tasting and digesting spicy foods containing capsaicin induce various physiological responses such as perspiration from face, salivation and facilitation of cardiovascular activity, which are thought to be caused through viscero-visceral autonomic reflexes. However, this does not necessarily exclude the possibility of the involvement of higher-order sensory-motor integration between the M/PSG and anterior short gyrus (ASG) known as the autonomic region of the insula. To reveal a possible functional coordination between the M/PSG and ASG, we here addressed whether capsaicin increases neural activity in the ASG as well as the M/PSG using fMRI and a custom-made taste delivery system. Twenty subjects participated in this study, and three tastant solutions: capsaicin, NaCl and artificial saliva (AS) were used. Group analyses with the regions activated by capsaicin revealed significant activations in the bilateral ASG and M/PSG. The fMRI blood oxygenation level-dependent (BOLD) signals in response to capsaicin stimulation were significantly higher in ASG than in M/PSG regardless of the side. Concomitantly, capsaicin increased the fingertip temperature significantly. Although there was no significant correlation between the fingertip temperatures and BOLD signals in the ASG or M/PSG when the contrast [Capsaicin–AS] or [Capsaicin–NaCl] was computed, a significant correlation was found in the bilateral ASG when the contrast [2×Capsaicin–NaCl–AS] was computed. In contrast, there was a significant correlation in the hypothalamus regardless of the contrasts. Furthermore, there was a significant correlation between M/PSG and ASG. These results indicate that capsaicin increases neural activity in the ASG as well as the M/PSG, suggesting that the neural coordination between the two cortical areas may be involved in autonomic responses to tasting spicy foods as reflected in fingertip temperature increases.
    Preview · Article · Jan 2016 · Frontiers in Human Neuroscience
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    • "The linear regression was used to reduce the effects of physiological processes (e.g., the fluctuations of cardiac and respiratory cycles). Otherwise, the 9 noise covariates were added in the regression analysis, including White Matter (WM), Cerebro-Spinal Fluid (CSF), Global Signal (GS), as well as 6 motion parameters (3 rotations and 3 translations as saved by the 3D motion correction) [39] [40] [41] [42]. We derived the GS/WM/CSF nuisance signals averaging the time courses of the voxels in each subject's whole brain/WM/CSF masks. "

    Full-text · Article · Oct 2015 · Neural Plasticity
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    • "Unfortunately, resting state EEG recordings do not have the sufficient spatial resolution to enlighten the functional connectivity between brain neural networks generating Rolandic mu rhythms and central autonomic network (CAN) supposed to adapt the activity of visceral organs according to animal data (Arthur and Loewy, 1990; Benarroch, 1993; Friedman and Thayer, 1998; Napadow et al., 2008; Saper, 2002; Ida and Llewellyn-Smith, 2011). It is supposed that CAN receives sensory afferents in medulla and integrate them in pons, thalamus, hypothalamus , amygdala, and insula. "
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    ABSTRACT: We tested the hypothesis of a relationship between heart rate variability (HRV) and Rolandic mu rhythms in relaxed condition of resting state. Resting state eyes-closed electroencephalographic (EEG) and electrocardiographic (ECG) data were recorded (10-20 system) in 42 healthy adults. EEG rhythms of interest were high-frequency alpha (10.5-13Hz) and low-frequency beta (13-20Hz), which are supposed to form Rolandic mu rhythms. Rolandic and occipital (control) EEG sources were estimated by LORETA software. Results showed a statistically significant (p<0.05, corrected) negative correlation across all subjects between Rolandic cortical sources of low-frequency beta rhythms and the low-frequency band power (LF, 0.04-0.15Hz) of tachogram spectrum as an index of HRV. The lower the amplitude of Rolandic sources of low-frequency beta rhythms (as a putative sign of activity of somatomotor cortex), the higher the LF band power of tachogram spectrum (as a putative sign of sympathetic activity). This effect was specific as there was neither a similar correlation between these EEG rhythms and high-frequency band power of tachogram spectrum (as a putative sign of parasympathetic vagal activity) neither between occipital sources of low-frequency beta rhythms (as a putative sign of activity of visual cortex) and LF band power of tachogram spectrum. These results suggest that Rolandic low-frequency beta rhythms are related to sympathetic activity regulating heart rate, as a dynamic neurophysiologic oscillatory mechanism sub-serving the interaction between brain neural populations involved in somatomotor control and brain neural populations regulating ANS signals to heart for on-going homeostatic adaptations. Copyright © 2015. Published by Elsevier B.V.
    Full-text · Article · Feb 2015 · International journal of psychophysiology: official journal of the International Organization of Psychophysiology
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