Review
A meta-analysis of heart rate variability and neuroimaging studies: Implications for heart rate variability as a marker of stress and health

https://doi.org/10.1016/j.neubiorev.2011.11.009Get rights and content

Abstract

The intimate connection between the brain and the heart was enunciated by Claude Bernard over 150 years ago. In our neurovisceral integration model we have tried to build on this pioneering work. In the present paper we further elaborate our model and update it with recent results. Specifically, we performed a meta-analysis of recent neuroimaging studies on the relationship between heart rate variability and regional cerebral blood flow. We identified a number of regions, including the amygdala and ventromedial prefrontal cortex, in which significant associations across studies were found. We further propose that the default response to uncertainty is the threat response and may be related to the well known negativity bias. Heart rate variability may provide an index of how strongly ‘top–down’ appraisals, mediated by cortical-subcortical pathways, shape brainstem activity and autonomic responses in the body. If the default response to uncertainty is the threat response, as we propose here, contextual information represented in ‘appraisal’ systems may be necessary to overcome this bias during daily life. Thus, HRV may serve as a proxy for ‘vertical integration’ of the brain mechanisms that guide flexible control over behavior with peripheral physiology, and as such provides an important window into understanding stress and health.

Highlights

► Examine relationship between heart rate variability and regional cerebral blood flow. ► Amygdala and the medial prefrontal cortex showed significant associations across studies. ► The default response to uncertainty is the threat response and may be related to the well known negativity bias.

Section snippets

Heart rate variability

Like many organs in the body, the heart is dually innervated. Although a wide range of physiologic factors determine cardiac functions such as heart rate (HR), the autonomic nervous system (ANS) is the most prominent. Importantly, when both cardiac vagal (the primary parasympathetic nerve) and sympathetic inputs are blocked pharmacologically (for example, with atropine plus propranolol, the so-called double blockade), intrinsic HR is higher than the normal resting HR (Jose and Collison, 1970).

Perceptions of threat and safety—the roles of the amygdala and the prefrontal cortex

What is stress? While researchers have debated the definition of stress for decades, perceptions of threat and safety appear to be a common, core element in “stressors” that are generated by mental events. Therefore, if HRV is to be considered as a potential marker of stress it needs to be tied to perceptions of threat and safety. These perceptions, and the associated actions that follow them, are important for the survival of the individual organism and ultimately of the species. As we argue

HRV and emotional regulation

In addition to being linked to vmPFC and amygdala modulation, emotion regulation is linked to HRV (Appelhans and Luecken, 2006, Thayer and Brosschot, 2005). Individuals with greater emotion regulation ability have been shown to have greater levels of resting HRV (Appelhans and Luecken, 2006, Thayer and Lane, 2009). In addition, during successful performance on emotion regulation tasks HRV appears to be increased (Butler et al., 2006, Ingjaldsson et al., 2003, Smith et al., 2011).

The ability to

Meta-analysis of neuroimaging studies of HRV

One of the basic ideas of the Neurovisceral Integration Model is that HRV is important not so much for what it tells us about the state of the heart as much as it is important for what it tells us about the state of the brain. Thus the extent to which HRV reflects important aspects of neural functioning is an empirically testable hypothesis associated with the model with critical implications for HRV as a marker of stress and resilience. Whereas a number of individual studies including

Neural structures associated with HRV

As part of the exposition of the Neurovisceral Integration Model we have previously described at set of neural structures associated with HRV (Thayer and Lane, 2000, Thayer and Lane, 2009). The various aspects of this network of neural structures have been gleaned from numerous sources including animal studies, human lesion studies, pharmacological blockade studies, and a few neuroimaging studies. Over the past several years however a number of human neuroimaging studies have appeared in which

Functional divisions of the medial PFC

To gain an understanding of the functional significance of the HRV-brain region associations identified in our meta-analysis it would be useful to know more about the functional subdivisions of mPFC and their differential role in cognitive and emotional processes. Though the subdivisions of the mPFC have been categorized in varying ways and a consensus on the functional boundaries and their definitive names has not yet been achieved, a number of useful schemes have been proposed. Bush et al.

Summary and conclusion

In the present paper we have presented a meta-analysis of studies relating cerebral blood flow to HRV. We have shown that several areas including the amygdala and the medial PFC that are involved in perceptions of threat and safety are also associated with HRV. The meta-analysis provides support for the idea that HRV may index the degree to which a mPFC-guided “core integration” system is integrated with the brainstem nuclei that directly regulate the heart. Thus these results support Claude

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