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Cardiac sympathetic-vagal activity initiates a functional brain-body response to emotional arousal.

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.

SUBMITTER: Candia-Rivera D

PROVIDER: S-EPMC9173754 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Cardiac sympathetic-vagal activity initiates a functional brain-body response to emotional arousal.

Candia-Rivera Diego D Catrambone Vincenzo V Thayer Julian F JF Gentili Claudio C Valenza Gaetano G

Proceedings of the National Academy of Sciences of the United States of America 20220519 21

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 tr ...[more]

PMID: 35588453

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Project description:Comorbid Lewy body pathology is very common in Alzheimer's disease and may confound clinical trial design, yet there is no in vivo test to identify patients with this. Tissue (and/or radioligand imaging) studies have shown cardiac sympathetic denervation in Parkinson's disease and dementia with Lewy bodies, but this has not been explored in Alzheimer's subjects with Lewy bodies not meeting dementia with Lewy bodies clinicopathological criteria. To determine if Alzheimer's disease with Lewy bodies subjects show sympathetic cardiac denervation, we analysed epicardial and myocardial tissue from autopsy-confirmed cases using tyrosine hydroxylase and neurofilament immunostaining. Comparison of tyrosine hydroxylase fibre density in 19 subjects with Alzheimer's disease/dementia with Lewy bodies, 20 Alzheimer's disease with Lewy bodies, 12 Alzheimer's disease subjects without Lewy body disease, 19 Parkinson's disease, 30 incidental Lewy body disease and 22 cognitively normal without Alzheimer's disease or Lewy body disease indicated a significant group difference (P < 0.01; Kruskal-Wallis analysis of variance) and subsequent pair-wise Mann-Whitney U tests showed that Parkinson's disease (P < 0.05) and Alzheimer's disease/dementia with Lewy bodies (P < 0.01) subjects, but not Alzheimer's disease with Lewy bodies subjects, had significantly reduced tyrosine hydroxylase fibre density as compared with cognitively normal. Both Parkinson's disease and Alzheimer's disease/dementia with Lewy bodies subjects also showed significant epicardial losses of neurofilament protein-immunoreactive nerve fibre densities within the fibre bundles as compared with cognitively normal subjects (P < 0.01) and both groups showed high pathologic alpha-synuclein densities (P < 0.0001). Cardiac alpha-synuclein densities correlated significantly with brain alpha-synuclein (P < 0.001), while cardiac tyrosine hydroxylase and neurofilament immunoreactive nerve fibre densities were negatively correlated with the densities of both brain and cardiac alpha-synuclein, as well as Unified Parkinson's Disease Rating Scale scores (P < 0.05). The clear separation of Alzheimer's disease/dementia with Lewy bodies subjects from Alzheimer's disease and cognitively normal, based on cardiac tyrosine hydroxylase fibre density, is the first report of a statistically significant difference between these groups. Our data do not show significant sympathetic cardiac denervation in Alzheimer's disease with Lewy bodies, but strongly confirm that cardiac nuclear imaging with a noradrenergic radioligand is worthy of further study as a potential means to separate Alzheimer's disease from Alzheimer's disease/dementia with Lewy bodies during life.

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Dataset Information

Cardiac sympathetic-vagal activity initiates a functional brain-body response to emotional arousal.

Publications

Cardiac sympathetic-vagal activity initiates a functional brain-body response to emotional arousal.

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