Effect of Parasympathetic Stimulation on Brain Activity During Appraisal of Fearful Expressions
Open accessAbstract
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.
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The dimensional model of interoception can be extended further to incorporate lower level measures of afferent neural traffic and the preconscious impact of interoceptive signals on sensory processing.
“This dimensional model of interoception can be extended further to incorporate lower level measures of afferent neural traffic (quantifying afferent signal strength, e.g. through heartbeat evoked potentials [20 ]), and the preconscious impact of interoceptive signals on sensory processing (e.g.modification of startle response [21 ,22] or augmentation of threat processing [23 ,24,25]).”
From Interoception and emotion. (2017) · cites this paper as [23]
The Discussion reports that carotid baroreceptor stimulation affected the processing and appraisal of fearful faces, supporting an impact of afferent signals on threat processing. But the paper's own findings describe attenuated, not augmented, responses to fearful faces during appraisal; it also does not establish that this effect was preconscious. (LLM, conf=0.86)
Experimental — accuracy not yet measuredA cardiac cycle by emotion interaction demonstrated enhanced bilateral amygdala activation in response to fear faces at systole.
“A cardiac cycle by emotion interaction demonstrated enhanced bilateral amygdala activation in response to fear faces at systole (b).”
From Interoception and emotion. (2017) · cites this paper as [23]
The Results section ('Interaction between carotid stimulation and emotional rating condition'; page unavailable) reports an emotion-by-stimulation interaction in the left amygdala during appraisal of fearful faces. It does not report a cardiac-cycle interaction or enhanced bilateral amygdala activation at systole; the reported effect was attenuation during carotid stimulation. (LLM, conf=0.86)
Experimental — accuracy not yet measuredBaroreceptor signals amplify threat processing, enhancing the detection and perception of fear signals in others.
“However, these baroreceptor signals amplify threat processing, enhancing the detection and perception of fear signals in others [23 ,24,25]”
From Interoception and emotion. (2017) · cites this paper as [23]
The Discussion (page unavailable) reports enhanced fear processing when stimuli coincide with natural baroreceptor firing during systole. But it also reports that this paper’s artificial carotid stimulation attenuated amygdala activity during appraisal of fearful faces. The unqualified claim that baroreceptor signals amplify threat processing therefore overstates what this source supports. (LLM, conf=0.85)
Experimental — accuracy not yet measuredCarotid artery stimulation leads to higher ratings of emotional expression intensity, and this increase for fearful faces is associated with decreased activation in the insula, amygdala, and periaqueductal grey area.
“carotid artery stimulation in this study led to higher ratings of emotional expression intensity, and this increase for fearful faces was associated with a decrease in activation in a number of brain areas including the insula, amygdala, and periaqueductal grey area.”
From Atypical interoception as a common risk factor for psychopathology: A review (2021) · cites this paper as Makovac et al., 2015
The Behavioural results section (page unavailable) reports higher intensity ratings with stimulation for neutral faces, but no overall increase for fearful faces; fearful-face ratings rose in some participants and fell in others. The Correlations with emotional ratings section links changes in fearful-face ratings to attenuation of activity in the insula, amygdala and periaqueductal grey area, but does not support describing that relationship simply as an increase in fearful-face ratings associated with decreased activation. (LLM, conf=0.88)
Experimental — accuracy not yet measured
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- Authors
- Makovac, E., Garfinkel, S. N., Bassi, A., Basile, B., Macaluso, E., Cercignani, M., Calcagnini, G., Mattei, E., Agalliu, D., Cortelli, P., Caltagirone, C., Bozzali, M., & Critchley, H.
- Affiliations
- Fondazione Santa Lucia (IT)
- Brighton and Sussex Medical School (GB)
- Istituto Superiore di Sanità (IT)
- University of Bologna (IT)
- University of Rome Tor Vergata (IT)
- Corresponding author
- Makovac, Elena
- ORCID
- Venue
- Neuropsychopharmacology
- Published
- 2015-01-12
- Volume
- 40
- Issue
- 7
- Pages
- 1649-1658
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC4915246
- OpenAlex
- W2014798867
- Semantic Scholar
- 809858f70a02b14eb476746b2dde6af39e0fd589
- Cited by
- 54
- References
- 64
- Citations by year
- 2026: 7 · 2025: 5 · 2024: 6 · 2023: 3 · 2022: 5 · 2021: 6 · 2020: 2 · 2019: 4 · 2018: 1 · 2017: 6 · 2016: 4 · 2015: 4
- FWCI
- 3.64
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Sussex Research Online (University of Sussex) (submittedVersion)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- Institutional Research Information System University of Turin (University of Turin) (submittedVersion)
- Funders
- University of Sussex (ERC-2012-ADG_20120411)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- parasympathetic nervous system, carotid baroreceptor stimulation, fear, amygdala, insula, hippocampus, heart rate variability, autonomic nervous system, emotional processing
- MeSH terms
- Adult, Analysis of Variance, Brain, Brain Mapping, Electric Stimulation, Facial Expression, Fear, Female, Heart Rate, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Oxygen, Parasympathetic Nervous System, Pattern Recognition, Visual, Young Adult
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