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Fear processing is differentially affected by lateralized stimulation of carotid baroreceptors

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posted on 2023-06-09, 07:10 authored by Elena Makovac, Sarah Garfinkel, Andrea Bassi, Barbara Basile, Emiliano Macaluso, Mara Cercignani, Giovanni Calcagnini, Eugenio Mattei, Daniela Agalliu, Pietro Cortelli, Carlo Caltagirone, Hugo CritchleyHugo Critchley, Marco Bozzali
Information processing, particularly of salient emotional stimuli, is influenced by cardiovascular afferent signals. Carotid baroreceptors signal the state of cardiovascular arousal to the brain, controlling blood pressure and heart rate via the baroreflex. Animal studies suggest a lateralization of this effect: Experimental stimulation of the right carotid sinus has a greater impact on heart rate when compared to left-sided stimulation. We tested, in humans, whether the processing of emotional information from faces was differentially affected by right versus left carotid afferents. To achieve so, we used an automated neck suction device to stimulate the carotid mechanoreceptors in the carotid sinus (parasympathetic pathway) synchronously with functional magnetic resonance imaging (fMRI) acquisition whilst participants were engaged in an emotional rating task of fearful and neutral faces. We showed that both right and left carotid stimulation influenced brain activity within opercular regions, although a stronger activation was observed within left insula during right stimulation compared to left stimulation. As regards the processing of fearful faces, right, but not left carotid stimulation attenuated the perceived intensity of fear, and (albeit to a lesser extent) enhanced intensity ratings of neutral faces. Mirroring the behavioural effects, there was a significant expression-by-stimulation interaction for right carotid stimulation only, when bilateral amygdala responses were attenuated to fear faces and amplified to neutral faces. Individual differences in basal heart rate variability (HRV) predicted the extent to which right carotid stimulation attenuated amygdala responses during fear processing. Our study provides unique evidence for lateralized viscerosensory effects on brain systems supporting emotional processing.

Funding

Cardiac control of fear in brain; G1120; EUROPEAN UNION; 324150 CCFIB

The Sackler Centre Donation; G0318; SACKLER-DR MORTIMER AND THERESA SACKLER FOUNDATION

History

Publication status

  • Published

File Version

  • Accepted version

Journal

Cortex

ISSN

0010-9452

Publisher

Elsevier

Volume

99

Page range

200-212

Department affiliated with

  • BSMS Neuroscience Publications

Research groups affiliated with

  • Sackler Centre for Consciousness Science Publications

Full text available

  • Yes

Peer reviewed?

  • Yes

Legacy Posted Date

2017-07-13

First Open Access (FOA) Date

2018-07-15

First Compliant Deposit (FCD) Date

2017-07-13

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