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

Elena Makovac, Sarah N. Garfinkel, Andrea Bassi, Barbara Basile, Emiliano Macaluso, Mara Cercignani, Giovanni Calcagnini, Eugenio Mattei, Daniela Agalliu, Pietro Cortelli, Carlo Caltagirone, Marco Bozzali, Hugo Critchley

Research output: Contribution to journalArticlepeer-review

Abstract

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.

Original languageEnglish
Pages (from-to)1649-1658
Number of pages10
JournalNeuropsychopharmacology
Volume40
Issue number7
DOIs
Publication statusPublished - Feb 4 2015

ASJC Scopus subject areas

  • Pharmacology
  • Psychiatry and Mental health

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