Intracranial Pressure Is a Determinant of Sympathetic Activity

Eric A Schmidt; Fabien Despas; Anne Pavy-Le Traon; Zofia Czosnyka; John D Pickard; Kamal Rahmouni; Atul Pathak; Jean M Senard

doi:10.3389/fphys.2018.00011

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Intracranial Pressure Is a Determinant of Sympathetic Activity

Journal article

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Intracranial Pressure Is a Determinant of Sympathetic Activity

Eric A Schmidt, Fabien Despas, Anne Pavy-Le Traon, Zofia Czosnyka, John D Pickard, Kamal Rahmouni, Atul Pathak and Jean M Senard

Frontiers in physiology, Vol.9, pp.11-11

02/08/2018

DOI: 10.3389/fphys.2018.00011

PMID: 29472865

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Abstract

Intracranial pressure (ICP) is the pressure within the cranium . ICP rise compresses brain vessels and reduces cerebral blood delivery. Massive ICP rise leads to cerebral ischemia, but it is also known to produce hypertension, bradycardia and respiratory irregularities due to a sympatho-adrenal mechanism termed Cushing response. One still unresolved question is whether the Cushing response is a non-synaptic acute brainstem ischemic mechanism or part of a larger physiological reflex for arterial blood pressure control and homeostasis regulation. We hypothesize that changes in ICP modulates sympathetic activity. Thus, modest ICP increase and decrease were achieved in mice and patients with respectively intra-ventricular and lumbar fluid infusion. Sympathetic activity was gauged directly by microneurography, recording renal sympathetic nerve activity in mice and muscle sympathetic nerve activity in patients, and gauged indirectly in both species by heart-rate variability analysis. In mice ( n = 15), renal sympathetic activity increased from 29.9 ± 4.0 bursts.s −1 (baseline ICP 6.6 ± 0.7 mmHg) to 45.7 ± 6.4 bursts.s −1 (plateau ICP 38.6 ± 1.0 mmHg) and decreased to 34.8 ± 5.6 bursts.s −1 (post-infusion ICP 9.1 ± 0.8 mmHg). In patients ( n = 10), muscle sympathetic activity increased from 51.2 ± 2.5 bursts.min −1 (baseline ICP 8.3 ± 1.0 mmHg) to 66.7 ± 2.9 bursts.min −1 (plateau ICP 25 ± 0.3 mmHg) and decreased to 58.8 ± 2.6 bursts.min −1 (post-infusion ICP 14.8 ± 0.9 mmHg). In patients 7 mmHg ICP rise significantly increases sympathetic activity by 17%. Heart-rate variability analysis demonstrated a significant vagal withdrawal during the ICP rise, in accordance with the microneurography findings. Mice and human results are alike. We demonstrate in animal and human that ICP is a reversible determinant of efferent sympathetic outflow, even at relatively low ICP levels. ICP is a biophysical stress related to the forces within the brain. But ICP has also to be considered as a physiological stressor, driving sympathetic activity. The results suggest a novel physiological ICP-mediated sympathetic modulation circuit and the existence of a possible intracranial (i.e., central) baroreflex. Modest ICP rise might participate to the pathophysiology of cardio-metabolic homeostasis imbalance with sympathetic over-activity, and to the pathogenesis of sympathetically-driven diseases.

translational medical research

Physiology

autonomic nervous system

intracranial pressure

baroreflex

microneurography

Details

Title: Subtitle: Intracranial Pressure Is a Determinant of Sympathetic Activity
Creators: Eric A Schmidt - Institut des Maladies Métaboliques et Cardiovasculaires, I2MC, Institut National de la Santé et de la Recherche Médicale, Université de Toulouse
Fabien Despas - Institut des Maladies Métaboliques et Cardiovasculaires, I2MC, Institut National de la Santé et de la Recherche Médicale, Université de Toulouse
Anne Pavy-Le Traon - Institut des Maladies Métaboliques et Cardiovasculaires, I2MC, Institut National de la Santé et de la Recherche Médicale, Université de Toulouse
Zofia Czosnyka - Brain Physics Lab, Academic Neurosurgery, University of Cambridge
John D Pickard - Brain Physics Lab, Academic Neurosurgery, University of Cambridge
Kamal Rahmouni - Departments of Pharmacology, University of Iowa
Atul Pathak - Institut des Maladies Métaboliques et Cardiovasculaires, I2MC, Institut National de la Santé et de la Recherche Médicale, Université de Toulouse
Jean M Senard - Institut des Maladies Métaboliques et Cardiovasculaires, I2MC, Institut National de la Santé et de la Recherche Médicale, Université de Toulouse
Resource Type: Journal article
Publication Details: Frontiers in physiology, Vol.9, pp.11-11
DOI: 10.3389/fphys.2018.00011
PMID: 29472865
NLM abbreviation: Front Physiol
ISSN: 1664-042X
eISSN: 1664-042X
Publisher: Frontiers Media S.A
Language: English
Date published: 02/08/2018
Academic Unit: Iowa Neuroscience Institute; Neuroscience and Pharmacology; Internal Medicine
Record Identifier: 9984040392802771

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