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Effect of parasympathetic stimulation on brain activity during appraisal of fearful expressions

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posted on 2023-06-08, 23:44 authored by Elena Makovac, Sarah Garfinkel, Andrea Bassi, Barbara Basile, Emiliano Macaluso, Mara Cercignani, Giovanni Calcagnini, Eugenio Mattei, Daniela Agalliu, Pietro Cortelli, Carlo Caltagirone, Marco Bozzali, Hugo CritchleyHugo Critchley
Autonomic nervous system activity is an important component of human emotion. Mental processes influence bodily physiology, which in turn feeds back to influence thoughts and feelings. Afferent cardiovascular signals from arterial baroreceptors in the carotid sinuses are processed within the brain and contribute to this two-way communication with the body. These carotid baroreceptors can be stimulated non-invasively by externally applying focal negative pressure bilaterally to the neck. In an experiment combining functional neuroimaging (fMRI) with carotid stimulation in healthy participants, we tested the hypothesis that manipulating afferent cardiovascular signals alters the central processing of emotional information (fearful and neutral facial expressions). Carotid stimulation, compared with sham stimulation, broadly attenuated activity across cortical and brainstem regions. Modulation of emotional processing was apparent as a significant expression-by-stimulation interaction within left amygdala, where responses during appraisal of fearful faces were selectively reduced by carotid stimulation. Moreover, activity reductions within insula, amygdala, and hippocampus correlated with the degree of stimulation-evoked change in the explicit emotional ratings of fearful faces. Across participants, individual differences in autonomic state (heart rate variability, a proxy measure of autonomic balance toward parasympathetic activity) predicted the extent to which carotid stimulation influenced neural (amygdala) responses during appraisal and subjective rating of fearful faces. Together our results provide mechanistic insight into the visceral component of emotion by identifying the neural substrates mediating cardiovascular influences on the processing of fear signals, potentially implicating central baroreflex mechanisms for anxiolytic treatment targets.

History

Publication status

  • Published

File Version

  • Accepted version

Journal

Neuropsychopharmacology

ISSN

0893-133X

Publisher

Nature Publishing Group

Issue

7

Volume

40

Page range

1649-1658

Department affiliated with

  • BSMS Neuroscience Publications

Full text available

  • Yes

Peer reviewed?

  • Yes

Legacy Posted Date

2015-12-14

First Open Access (FOA) Date

2015-12-14

First Compliant Deposit (FCD) Date

2015-12-14

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