title: Effect of parasympathetic stimulation on brain activity during appraisal of fearful expressions.
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.
authors.affiliation: Neuroimaging Laboratory, IRCCS Santa Lucia Foundation, Rome, Italy.
authors.forename: Elena
authors.initials: E
authors.lastname: Makovac
authors.affiliation: 1] Psychiatry, Brighton and Sussex Medical School, University of Sussex, Falmer, Brighton, UK [2] Sackler Centre for Consciousness Science, University of Sussex, Falmer, Brighton, UK.
authors.forename: Sarah N
authors.initials: SN
authors.lastname: Garfinkel
authors.affiliation: Department of Clinical and Behavioural Neurology, IRCCS Santa Lucia Foundation, Rome, Italy.
authors.forename: Andrea
authors.initials: A
authors.lastname: Bassi
authors.affiliation: Neuroimaging Laboratory, IRCCS Santa Lucia Foundation, Rome, Italy.
authors.forename: Barbara
authors.initials: B
authors.lastname: Basile
authors.affiliation: Neuroimaging Laboratory, IRCCS Santa Lucia Foundation, Rome, Italy.
authors.forename: Emiliano
authors.initials: E
authors.lastname: Macaluso
authors.affiliation: 1] Neuroimaging Laboratory, IRCCS Santa Lucia Foundation, Rome, Italy [2] Brighton & Sussex Medical School, Clinical Imaging Sciences Centre, University of Sussex, Brighton, UK.
authors.forename: Mara
authors.initials: M
authors.lastname: Cercignani
authors.affiliation: Department of Technology and Health, Italian Institute of Health, Rome, Italy.
authors.forename: Giovanni
authors.initials: G
authors.lastname: Calcagnini
authors.affiliation: Department of Technology and Health, Italian Institute of Health, Rome, Italy.
authors.forename: Eugenio
authors.initials: E
authors.lastname: Mattei
authors.affiliation: Department of Clinical and Behavioural Neurology, IRCCS Santa Lucia Foundation, Rome, Italy.
authors.forename: Daniela
authors.initials: D
authors.lastname: Agalliu
authors.affiliation: 1] Neurological Clinic, DIBIDEM, Alma Mater Studiorum-University of Bologna, Bologna, Italy [2] IRCCS Institute of Neurological Sciences of Bologna, Bologna, Italy.
authors.forename: Pietro
authors.initials: P
authors.lastname: Cortelli
authors.affiliation: 1] Department of Clinical and Behavioural Neurology, IRCCS Santa Lucia Foundation, Rome, Italy [2] Department of Neuroscience, University of Rome 'Tor Vergata', Rome, Italy.
authors.forename: Carlo
authors.initials: C
authors.lastname: Caltagirone
authors.affiliation: Neuroimaging Laboratory, IRCCS Santa Lucia Foundation, Rome, Italy.
authors.forename: Marco
authors.initials: M
authors.lastname: Bozzali
authors.affiliation: 1] Psychiatry, Brighton and Sussex Medical School, University of Sussex, Falmer, Brighton, UK [2] Sackler Centre for Consciousness Science, University of Sussex, Falmer, Brighton, UK.
authors.forename: Hugo
authors.initials: H
authors.lastname: Critchley
mesh_terms: D000328:Adult; D000704:Analysis of Variance; D001921:Brain / Q000098:blood supply / Q000502:physiology*; D001931:Brain Mapping; D004558:Electric Stimulation / Q000379:methods*; D005149:Facial Expression; D005239:Fear; D005260:Female; D006339:Heart Rate / Q000502:physiology; D006801:Humans; D007091:Image Processing, Computer-Assisted; D008279:Magnetic Resonance Imaging; D008297:Male; D010100:Oxygen / Q000097:blood; D010275:Parasympathetic Nervous System / Q000502:physiology*; D010364:Pattern Recognition, Visual; D055815:Young Adult
chemical_list: D010100:Oxygen