2006 Heart-Brain summit proceedings
The little brain on the heart
ARTICLE INTRODUCTION
The function of the cardiovascular neuronal hierarchy is ultimately to match cardiac output to regional body blood flow demands. To comprehend how the varied elements of this hierarchy interact to accomplish this task, we must determine how its peripheral (intrathoracic and cervical ganglion) and central neurons communicate on an ongoing basis in the coordination of regional cardiac indices.
The cardiac neuronal hierarchy can be represented as a massively parallel and, for the most part, stochastic control system such that stable cardiac control generally occurs in the absence of obvious cause and effect (see sidebar below). Its peripheral neuronal interactions display emergent properties, functioning as they normally do in a highly optimized fashion to tolerate normal cardiac perturbations.
From a clinical perspective, excessive activation of select elements within the cardiac neuronal hierarchy has been thought to result in the genesis of atrial or ventricular arrhythmias. Indeed, the functional interconnectivity of the various neurons in the hierarchy is so organized that the whole can be catastrophically disabled by cascading failures initiated by relatively minor abnormal inputs. Defining the function of each of its populations may be required to understand how, for instance, excessive activation of select elements initiates cardiac arrhythmias. Such an understanding is required if one is to manage this state from a neurocardiological perspective.
This brief review presents the anatomy and function of this hierarchy’s afferent and efferent neurons and discusses the putative interactions that occur among its neuronal populations.
CITATIONS
- Armour JA.
Anatomy and function of the intrathoracic neurons regulating the mammalian heart. In: Zucker IH, Gilmore JP, eds. Reflex Control of the Circulation. Boca Raton, FL: CRC Press; 1991:1–37. - Armour JA, Richer L-P, Pagé P, et al.
Origin and pharmacological response of atrial tachyarrhythmias induced by discrete activation of mediastinal nerves in canines. Auton Neurosci 2005; 118:68–78.
http://www.ncbi.nlm.nih.gov/pubmed/15795179 - Huang MH, Wolf SG, Armour J.
Ventricular arrhythmias induced by chemically modified intrinsic cardiac neurons. Cardiovasc Res 1994; 28:636–642.
http://www.ncbi.nlm.nih.gov/pubmed/7517790 - Sylvén C.
The genesis of pain during myocardial ischemia and infarction. In: Armour JA, Ardell JL, eds. Basic and Clinical Neurocardiology. Oxford, UK: Oxford University Press; 2004:298–314. - Vance WH, Bowker RC.
Spinal origins of cardiac afferents from the region of the left anterior descending artery. Brain Res 1983; 258:96–100. - Cheng Z, Powley TL, Schwaber JS, Doyle FJ.
Vagal afferent innervation of the atria of the rat heart reconstructed with confocal microscopy. J Comp Neurol 1997; 381:1–17.
http://www.ncbi.nlm.nih.gov/pubmed/9087415 - McAllen RM, Spyer KM.
The location of cardiac vagal preganglionic motorneurons in the medulla of the cat. J Physiol 1976; 258:187–204.
http://www.ncbi.nlm.nih.gov/pubmed/940054 - Hopkins DA, Armour JA.
Localization of sympathetic postganglionic and parasympathetic preganglionic neurons which innervate different regions of the dog heart. J Comp Neurol 1984; 229:186–198.
http://www.ncbi.nlm.nih.gov/pubmed/6501600 - Gray AL, Johnson CI, Ardell JL, Massari VJ.
Parasympathetic control of the heart. A novel interganglionic intrinsic cardiac circuit mediates neural control of the heart. J Applied Physiol 2004; 96:2273–2278.
http://www.ncbi.nlm.nih.gov/pubmed/14978001 - Norris JE, Lippincott D, Wurster RD.
Responses of canine endocardium to stimulation of upper thoracic roots. Am J Physiol 1977; 233:H655–H659.
http://www.ncbi.nlm.nih.gov/pubmed/596462 - Darvesh S, Nance DM, Hopkins DA, Armour JA.
Distribution of neuropeptide immunoreactivity in intact and chronically decentralized middle cervical and stellate ganglia of dogs. J Autonom Nerv Syst 1987; 21:167–180.
http://www.ncbi.nlm.nih.gov/pubmed/2453549 - Horackova M, Armour JA, Byczko Z.
Multiple neurochemical coding of intrinsic cardiac neurons in whole-mount guinea-pig atria; confocal microscopic study. Cell Tissue Res 1999; 297:409–421.
http://www.ncbi.nlm.nih.gov/pubmed/10460488 - Singh S, Johnson PI, Gray TS, Lonchyna VA, Wurster RD.
Monamine- and histamine-synthesizing enzymes and neurotransmitters within neurons in adult human cardiac ganglia. Circulation 1999; 99:411–419.
http://www.ncbi.nlm.nih.gov/pubmed/9918529 - Armour JA, Kember GC.
Cardiac sensory neurons. In: Armour JA, Ardell JL, eds. Basic and Clinical Neurocardiology. Oxford, UK: Oxford University Press; 2004:79–117. - Malliani A.
Cardiovascular sympathetic afferent fibers. Rev Physiol Biochem Pharmacol 1982; 94:11–74. - Thorén P.
Role of cardiac vagal c-fibers in cardiovascular control. Rev Physiol Biochem Pharmacol 1979; 86:1–94.
http://www.ncbi.nlm.nih.gov/pubmed/386467 - Rubio R, Berne RM, Katori M.
Release of adenosine in reactive hyperemia of the dog heart. Am J Physiol 1969; 216:56–62.
http://www.ncbi.nlm.nih.gov/pubmed/5765591 - Andresen MC, Kuntz DL, Mendelowitz D.
Central nervous system regulation of the heart. In: Armour JA, Ardell JL, eds. Basic and Clinical Neurocardiology. Oxford, UK: Oxford University Press; 2004:187–219. - Levy MN, Martin PJ.
Neural control of the heart. In: Berne RM, ed. Handbook of Physiology: The Cardiovascular System. Bethesda, MD: American Physiological Society; 1979:581–620. - Ardell JL.
Anatomy and function of mammalian intrinsic cardiac neurons. In: Armour JA, Ardell JL, eds. Neurocardiology. New York, NY: Oxford University Press; 1994:95–114. - Randall WC, Wurster RD, Randall DC, Xi-Moy S.
From cardioaccelerator and inhibitory nerves to a heart brain: an evolution of concepts. In: Shepherd JT, Vatner SF, eds. Nervous Control of theHeart. Amsterdam: Harwood Academic Publishers; 1996:173–200.