Abstract

The neurovisceral integration model has shown a key role of the amygdala in neural circuits underlying heart rate variability (HRV) modulation, and suggested that reciprocal connections from amygdala to brain regions centered on the central autonomic network (CAN) are associated with HRV. To provide neuroanatomical evidence for these theoretical perspectives, the current study used covariance analysis of MRI-based gray matter volume (GMV) to map structural covariance network of the amygdala, and then determined whether the interregional structural correlations related to individual differences in HRV. The results showed that covariance patterns of the amygdala encompassed large portions of cortical (e.g., prefrontal, cingulate, and insula) and subcortical (e.g., striatum, hippocampus, and midbrain) regions, lending evidence from structural covariance analysis to the notion that the amygdala was a pivotal node in neural pathways for HRV modulation. Importantly, participants with higher resting HRV showed increased covariance of amygdala to dorsal medial prefrontal cortex and anterior cingulate cortex (dmPFC/dACC) extending into adjacent medial motor regions [i.e., pre-supplementary motor area (pre-SMA)/SMA], demonstrating structural covariance of the prefrontal-amygdala pathways implicated in HRV, and also implying that resting HRV may reflect the function of neural circuits underlying cognitive regulation of emotion as well as facilitation of adaptive behaviors to emotion. Our results, thus, provide anatomical substrates for the neurovisceral integration model that resting HRV may index an integrative neural network which effectively organizes emotional, cognitive, physiological and behavioral responses in the service of goal-directed behavior and adaptability.

Highlights

  • Previous neuroimaging studies have advanced our understanding of the neural correlates of heart rate variability (HRV), providing convergent evidence for activation in neural structures of the central autonomic network (CAN) involved in HRV modulation (Benarroch, 1993; Thayer and Lane, 2009; Thayer et al, 2012; Beissner et al, 2013)

  • Based on covariance analysis of structural MRI-based gray matter volume (GMV) measurements, we assessed the relationship between structural brain network of amygdala and individual differences in resting HRV

  • The results showed widespread structural correlations of amygdala to cortical and subcortical regions, extending previous tract tracing and functional connectivity results to the domain of interregional structural covariance patterns in the brain, suggesting that the amygdala serves as a crucial node in neural circuits underlying HRV regulation (Thayer and Lane, 2009; Thayer et al, 2012)

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Summary

Introduction

Previous neuroimaging studies have advanced our understanding of the neural correlates of heart rate variability (HRV), providing convergent evidence for activation in neural structures of the central autonomic network (CAN) involved in HRV modulation (Benarroch, 1993; Thayer and Lane, 2009; Thayer et al, 2012; Beissner et al, 2013). Sakaki et al (2016) revealed that higher resting HRV was related to stronger functional connectivity between amygdala and mPFC, potentially reflecting more efficient communication between amygdala and mPFC in individuals with greater HRV These findings demonstrate that functional connections between prefrontal cortex and amygdala covary with individual difference in baseline HRV, and suggest that taking a network perspective on neural correlates of HRV could be better understanding of the neurovisceral integration model. It remains unclear whether the underlying anatomical connections between prefrontal cortex and amygdala and/or other components of the CAN (e.g., insula and midbrain) are associated with HRV.

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