Brain-Heart interplay in emotional arousal - resolving a hundred year old debate

Candia-Rivera et al. do a fascinating piece of work that answers some long-standing issues in the century old debate on the role of the autonomic nervous system in feelings. I will be slowly re-reading this paper a number of times. The introduction provides an excellent review of contrasting theories of what emotions are.

...The debate about the role of the ANS in emotions can be condensed into two views: specificity or causation. The specificity view is related to the James–Lange theory, which states that bodily responses precede emotions’ central processing, meaning that bodily states would be a response to the environment, followed by an interpretation carried out by the CNS that would result in the feeling felt. However, causation theories represent an updated view of the James–Lange theory, suggesting that peripheral changes influence the conscious emotional experience....While more “classical” theories point to emotions as “the functional states of the brain that provide causal explanations of certain complex behaviors—like evading a predator or attacking prey”, other theories suggest how they are constructions of the world, not reactions to it (see MindBlog posts on Lisa Feldman Barretts work). Namely, emotions are internal states constructed on the basis of previous experiences as predictive schemes to react to external stimuli.

Here is a clip from the discussion of their open source paper, followed by the significance and abstract sections at the begninning of the article:

....To the best of our knowledge, major novelties of the current study with respect to prior state of the art are related to 1) the uncovering of the directed functional interplay between central and peripheral neural dynamics during an emotional elicitation, using ad-hoc mathematical models for synchronized EEG and ECG time series; 2) the uncovering of temporal dynamics of cortical and cardiovascular neural control during emotional processing in both ascending, from the heart to the brain, and descending, from the brain to the heart, functional directions; and 3) the experimental support for causation theories of physiological feelings.

In the frame of investigating the visceral origin of emotions, main findings of this study suggest that ascending BHI (brain-heart interplay) coupling initiates emotional processing and is mainly modulated by the subjective experience of emotional arousal. Such a relationship between arousal and ascending BHI may not be related to the attention levels, as controlled with two different neural correlates of attention. The main interactions begin through afferent vagal pathways (HF power) sustaining EEG oscillations, in which the theta band was repeatedly found related to major vagal modulations. In turn, with a later onset, this ascending modulation actually triggers a cascade of cortical neural activations that, in turn, modulate directed neural control onto the heart, namely from-brain-to-heart interplay. Concurrent bidirectional communication between the brain and body occurs throughout the emotional processing at specific timings, reaching a maximum coupling around 15 to 20 s from the elicitation onset, involving both cardiac sympathetic and vagal activity.

From the beginning of the article;  

Significance

We investigate the temporal dynamics of brain and cardiac activities in healthy subjects who underwent an emotional elicitation through videos. We demonstrate that, within the first few seconds, emotional stimuli modulate heartbeat activity, which in turn stimulates an emotion intensity (arousal)–specific cortical response. The emotional processing is then sustained by a bidirectional brain–heart interplay, where the perceived arousal level modulates the amplitude of ascending heart-to-brain neural information flow. These findings may constitute fundamental knowledge linking neurophysiology and psychiatric disorders, including the link between depressive symptoms and cardiovascular disorders.

Abstract

A century-long debate on bodily states and emotions persists. While the involvement of bodily activity in emotion physiology is widely recognized, the specificity and causal role of such activity related to brain dynamics has not yet been demonstrated. We hypothesize that the peripheral neural control on cardiovascular activity prompts and sustains brain dynamics during an emotional experience, so these afferent inputs are processed by the brain by triggering a concurrent efferent information transfer to the body. To this end, we investigated the functional brain–heart interplay under emotion elicitation in publicly available data from 62 healthy subjects using a computational model based on synthetic data generation of electroencephalography and electrocardiography signals. Our findings show that sympathovagal activity plays a leading and causal role in initiating the emotional response, in which ascending modulations from vagal activity precede neural dynamics and correlate to the reported level of arousal. The subsequent dynamic interplay observed between the central and autonomic nervous systems sustains the processing of emotional arousal. These findings should be particularly revealing for the psychophysiology and neuroscience of emotions.