Brain-Heart Pathways to Blood Pressure-Related Hypoalgesia

Cristina Ottaviani, Sabrina Fagioli, Eugenio Mattei, Federica Censi, Louisa Edwards, Emiliano Macaluso, Marco Bozzali, Hugo D. Critchley, Giovanni Calcagnini

Research output: Contribution to journalArticle

Abstract

OBJECTIVE: High blood pressure (BP) is associated with reduced pain sensitivity, known as BP-related hypoalgesia. The underlying neural mechanisms remain uncertain, yet arterial baroreceptor signaling, occurring at cardiac systole, is implicated. We examined normotensives using functional neuroimaging and pain stimulation during distinct phases of the cardiac cycle to test the hypothesized neural mediation of baroreceptor-induced attenuation of pain. METHODS: Eighteen participants (10 women; 32.7 (6.5) years) underwent BP monitoring for 1 week at home, and individual pain thresholds were determined in the laboratory. Subsequently, participants were administered unpredictable painful and nonpainful electrocutaneous shocks (stimulus type), timed to occur either at systole or at diastole (cardiac phase) in an event-related design. After each trial, participants evaluated their subjective experience. RESULTS: Subjective pain was lower for painful stimuli administered at systole compared with diastole, F(1, 2283) = 4.82, p = 0.03. Individuals with higher baseline BP demonstrated overall lower pain perception, F(1, 2164) = 10.47, p <.0001. Within the brain, painful stimulation activated somatosensory areas, prefrontal cortex, cingulate cortex, posterior insula, amygdala, and the thalamus. Stimuli delivered during systole (concurrent with baroreceptor discharge) activated areas associated with heightened parasympathetic drive. No stimulus type by cardiac phase interaction emerged except for a small cluster located in the right parietal cortex. CONCLUSIONS: We confirm the negative associations between BP and pain, highlighting the antinociceptive impact of baroreceptor discharge. Neural substrates associated with baroreceptor/BP-related hypoalgesia include superior parietal lobule, precentral, and lingual gyrus, regions typically involved in the cognitive aspects of pain experience.
Original languageEnglish
Pages (from-to)845-852
Number of pages8
JournalPsychosomatic Medicine
Volume80
Issue number9
DOIs
Publication statusPublished - Nov 1 2018

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Pressoreceptors
Systole
Blood Pressure
Pain
Brain
Parietal Lobe
Diastole
Hypertension
Occipital Lobe
Functional Neuroimaging
Pain Perception
Pain Threshold
Gyrus Cinguli
Frontal Lobe
Amygdala
Prefrontal Cortex
Thalamus
Shock

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Brain-Heart Pathways to Blood Pressure-Related Hypoalgesia. / Ottaviani, Cristina; Fagioli, Sabrina; Mattei, Eugenio; Censi, Federica; Edwards, Louisa; Macaluso, Emiliano; Bozzali, Marco; Critchley, Hugo D.; Calcagnini, Giovanni.

In: Psychosomatic Medicine, Vol. 80, No. 9, 01.11.2018, p. 845-852.

Research output: Contribution to journalArticle

Ottaviani, C, Fagioli, S, Mattei, E, Censi, F, Edwards, L, Macaluso, E, Bozzali, M, Critchley, HD & Calcagnini, G 2018, 'Brain-Heart Pathways to Blood Pressure-Related Hypoalgesia', Psychosomatic Medicine, vol. 80, no. 9, pp. 845-852. https://doi.org/10.1097/PSY.0000000000000581
Ottaviani, Cristina ; Fagioli, Sabrina ; Mattei, Eugenio ; Censi, Federica ; Edwards, Louisa ; Macaluso, Emiliano ; Bozzali, Marco ; Critchley, Hugo D. ; Calcagnini, Giovanni. / Brain-Heart Pathways to Blood Pressure-Related Hypoalgesia. In: Psychosomatic Medicine. 2018 ; Vol. 80, No. 9. pp. 845-852.
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AU - Ottaviani, Cristina

AU - Fagioli, Sabrina

AU - Mattei, Eugenio

AU - Censi, Federica

AU - Edwards, Louisa

AU - Macaluso, Emiliano

AU - Bozzali, Marco

AU - Critchley, Hugo D.

AU - Calcagnini, Giovanni

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N2 - OBJECTIVE: High blood pressure (BP) is associated with reduced pain sensitivity, known as BP-related hypoalgesia. The underlying neural mechanisms remain uncertain, yet arterial baroreceptor signaling, occurring at cardiac systole, is implicated. We examined normotensives using functional neuroimaging and pain stimulation during distinct phases of the cardiac cycle to test the hypothesized neural mediation of baroreceptor-induced attenuation of pain. METHODS: Eighteen participants (10 women; 32.7 (6.5) years) underwent BP monitoring for 1 week at home, and individual pain thresholds were determined in the laboratory. Subsequently, participants were administered unpredictable painful and nonpainful electrocutaneous shocks (stimulus type), timed to occur either at systole or at diastole (cardiac phase) in an event-related design. After each trial, participants evaluated their subjective experience. RESULTS: Subjective pain was lower for painful stimuli administered at systole compared with diastole, F(1, 2283) = 4.82, p = 0.03. Individuals with higher baseline BP demonstrated overall lower pain perception, F(1, 2164) = 10.47, p <.0001. Within the brain, painful stimulation activated somatosensory areas, prefrontal cortex, cingulate cortex, posterior insula, amygdala, and the thalamus. Stimuli delivered during systole (concurrent with baroreceptor discharge) activated areas associated with heightened parasympathetic drive. No stimulus type by cardiac phase interaction emerged except for a small cluster located in the right parietal cortex. CONCLUSIONS: We confirm the negative associations between BP and pain, highlighting the antinociceptive impact of baroreceptor discharge. Neural substrates associated with baroreceptor/BP-related hypoalgesia include superior parietal lobule, precentral, and lingual gyrus, regions typically involved in the cognitive aspects of pain experience.

AB - OBJECTIVE: High blood pressure (BP) is associated with reduced pain sensitivity, known as BP-related hypoalgesia. The underlying neural mechanisms remain uncertain, yet arterial baroreceptor signaling, occurring at cardiac systole, is implicated. We examined normotensives using functional neuroimaging and pain stimulation during distinct phases of the cardiac cycle to test the hypothesized neural mediation of baroreceptor-induced attenuation of pain. METHODS: Eighteen participants (10 women; 32.7 (6.5) years) underwent BP monitoring for 1 week at home, and individual pain thresholds were determined in the laboratory. Subsequently, participants were administered unpredictable painful and nonpainful electrocutaneous shocks (stimulus type), timed to occur either at systole or at diastole (cardiac phase) in an event-related design. After each trial, participants evaluated their subjective experience. RESULTS: Subjective pain was lower for painful stimuli administered at systole compared with diastole, F(1, 2283) = 4.82, p = 0.03. Individuals with higher baseline BP demonstrated overall lower pain perception, F(1, 2164) = 10.47, p <.0001. Within the brain, painful stimulation activated somatosensory areas, prefrontal cortex, cingulate cortex, posterior insula, amygdala, and the thalamus. Stimuli delivered during systole (concurrent with baroreceptor discharge) activated areas associated with heightened parasympathetic drive. No stimulus type by cardiac phase interaction emerged except for a small cluster located in the right parietal cortex. CONCLUSIONS: We confirm the negative associations between BP and pain, highlighting the antinociceptive impact of baroreceptor discharge. Neural substrates associated with baroreceptor/BP-related hypoalgesia include superior parietal lobule, precentral, and lingual gyrus, regions typically involved in the cognitive aspects of pain experience.

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