The Autonomic Brain: an Activation Likelihood Estimation Meta-analysis for Central Processing of Autonomic Function

Overview

Journal J Neurosci

Specialty Neurology

Date 2013 Jun 21

PMID 23785162

Citations 359

Authors

Florian Beissner

Karin Meissner

Karl-Jurgen Bar

Vitaly Napadow

Affiliations

Soon will be listed here.

Abstract

The autonomic nervous system (ANS) is of paramount importance for daily life. Its regulatory action on respiratory, cardiovascular, digestive, endocrine, and many other systems is controlled by a number of structures in the CNS. While the majority of these nuclei and cortices have been identified in animal models, neuroimaging studies have recently begun to shed light on central autonomic processing in humans. In this study, we used activation likelihood estimation to conduct a meta-analysis of human neuroimaging experiments evaluating central autonomic processing to localize (1) cortical and subcortical areas involved in autonomic processing, (2) potential subsystems for the sympathetic and parasympathetic divisions of the ANS, and (3) potential subsystems for specific ANS responses to different stimuli/tasks. Across all tasks, we identified a set of consistently activated brain regions, comprising left amygdala, right anterior and left posterior insula and midcingulate cortices that form the core of the central autonomic network. While sympathetic-associated regions predominate in executive- and salience-processing networks, parasympathetic regions predominate in the default mode network. Hence, central processing of autonomic function does not simply involve a monolithic network of brain regions, instead showing elements of task and division specificity.

Citing Articles

Myocardial injury in spontaneous intracerebral hemorrhage is not predicted by prior cardiac disease or neurological status: results from the Mannheim Stroke database.

Lesch H, Haucke L, Kruska M, Ebert A, Becker L, Szabo K Front Neurol. 2025; 16:1510361.

PMID: 40040916 PMC: 11876033. DOI: 10.3389/fneur.2025.1510361.

The brain-heart axis: integrative cooperation of neural, mechanical and biochemical pathways.

Valenza G, Matic Z, Catrambone V Nat Rev Cardiol. 2025; .

PMID: 40033035 DOI: 10.1038/s41569-025-01140-3.

A new directionality index based on high-resolution joint symbolic dynamics to assess information transfer in multivariate networks.

Schulz S, Schumann A, Bar K, Haueisen J, Seifert G, Voss A Front Neurosci. 2025; 19:1504161.

PMID: 40018361 PMC: 11865042. DOI: 10.3389/fnins.2025.1504161.

Characterizing Brain-Cardiovascular Aging Using Multiorgan Imaging and Machine Learning.

Amirmoezzi Y, Cropley V, Mansour L S, Seguin C, Zalesky A, Tian Y J Neurosci. 2025; 45(8).

PMID: 39971581 PMC: 11841759. DOI: 10.1523/JNEUROSCI.1440-24.2024.

Evidence for domain-general arousal from semantic and neuroimaging meta-analyses reconciles opposing views on arousal.

Sabat M, de Dampierre C, Tallon-Baudry C Proc Natl Acad Sci U S A. 2025; 122(6):e2413808122.

PMID: 39899711 PMC: 11831115. DOI: 10.1073/pnas.2413808122.

References

Williams L, Phillips M, Brammer M, Skerrett D, Lagopoulos J, Rennie C . Arousal dissociates amygdala and hippocampal fear responses: evidence from simultaneous fMRI and skin conductance recording. Neuroimage. 2001; 14(5):1070-9. DOI: 10.1006/nimg.2001.0904. View

Suzuki H, Watanabe S, Hamaguchi T, Mine H, Terui T, Kanazawa M . Brain activation associated with changes in heart rate, heart rate variability, and plasma catecholamines during rectal distention. Psychosom Med. 2009; 71(6):619-26. DOI: 10.1097/PSY.0b013e31819b69ca. View

Goswami R, Frances M, Shoemaker J . Representation of somatosensory inputs within the cortical autonomic network. Neuroimage. 2010; 54(2):1211-20. DOI: 10.1016/j.neuroimage.2010.09.050. View

Beckmann C, DeLuca M, Devlin J, Smith S . Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci. 2005; 360(1457):1001-13. PMC: 1854918. DOI: 10.1098/rstb.2005.1634. View

Craig A . Forebrain emotional asymmetry: a neuroanatomical basis?. Trends Cogn Sci. 2005; 9(12):566-71. DOI: 10.1016/j.tics.2005.10.005. View

Koelsch S, Remppis A, Sammler D, Jentschke S, Mietchen D, Fritz T . A cardiac signature of emotionality. Eur J Neurosci. 2007; 26(11):3328-38. DOI: 10.1111/j.1460-9568.2007.05889.x. View

Ito H, Yokoyama I, Tamura Y, Kinoshita T, Hatazawa J, Kawashima R . Regional changes in human cerebral blood flow during dipyridamole stress: neural activation in the thalamus and prefrontal cortex. Neuroimage. 2002; 16(3 Pt 1):788-93. DOI: 10.1006/nimg.2002.1123. View

Marci C, Glick D, Loh R, Dougherty D . Autonomic and prefrontal cortex responses to autobiographical recall of emotions. Cogn Affect Behav Neurosci. 2007; 7(3):243-50. DOI: 10.3758/cabn.7.3.243. View

Knight D, Nguyen H, Bandettini P . The role of the human amygdala in the production of conditioned fear responses. Neuroimage. 2005; 26(4):1193-200. DOI: 10.1016/j.neuroimage.2005.03.020. View

10.

Urry H, van Reekum C, Johnstone T, Davidson R . Individual differences in some (but not all) medial prefrontal regions reflect cognitive demand while regulating unpleasant emotion. Neuroimage. 2009; 47(3):852-63. PMC: 2766667. DOI: 10.1016/j.neuroimage.2009.05.069. View

11.

Vogt B, Finch D, Olson C . Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb Cortex. 1992; 2(6):435-43. DOI: 10.1093/cercor/2.6.435-a. View

12.

Burton A, Birznieks I, Bolton P, Henderson L, Macefield V . Effects of deep and superficial experimentally induced acute pain on muscle sympathetic nerve activity in human subjects. J Physiol. 2008; 587(1):183-93. PMC: 2670032. DOI: 10.1113/jphysiol.2008.162230. View

13.

Mufson E, Mesulam M . Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum. J Comp Neurol. 1982; 212(1):23-37. DOI: 10.1002/cne.902120103. View

14.

Kimmerly D, OLeary D, Menon R, Gati J, Shoemaker J . Cortical regions associated with autonomic cardiovascular regulation during lower body negative pressure in humans. J Physiol. 2005; 569(Pt 1):331-45. PMC: 1464214. DOI: 10.1113/jphysiol.2005.091637. View

15.

Cechetto D, Shoemaker J . Functional neuroanatomy of autonomic regulation. Neuroimage. 2009; 47(3):795-803. DOI: 10.1016/j.neuroimage.2009.05.024. View

16.

Williams L, Brown K, Das P, Boucsein W, Sokolov E, Brammer M . The dynamics of cortico-amygdala and autonomic activity over the experimental time course of fear perception. Brain Res Cogn Brain Res. 2004; 21(1):114-23. DOI: 10.1016/j.cogbrainres.2004.06.005. View

17.

Critchley H, Nagai Y, Gray M, Mathias C . Dissecting axes of autonomic control in humans: Insights from neuroimaging. Auton Neurosci. 2010; 161(1-2):34-42. DOI: 10.1016/j.autneu.2010.09.005. View

18.

Anderson E, Sinkey C, Mark A . Mental stress increases sympathetic nerve activity during sustained baroreceptor stimulation in humans. Hypertension. 1991; 17(4 Suppl):III43-9. DOI: 10.1161/01.hyp.17.4_suppl.iii43. View

19.

Evans K, Dougherty D, Schmid A, Scannell E, McCallister A, Benson H . Modulation of spontaneous breathing via limbic/paralimbic-bulbar circuitry: an event-related fMRI study. Neuroimage. 2009; 47(3):961-71. PMC: 3752895. DOI: 10.1016/j.neuroimage.2009.05.025. View

20.

Seeley W, Menon V, Schatzberg A, Keller J, Glover G, Kenna H . Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci. 2007; 27(9):2349-56. PMC: 2680293. DOI: 10.1523/JNEUROSCI.5587-06.2007. View