Pharmacological Reviews, Vol 21, 247-324, Copyright © 1969 by the American Society for Pharmacology and Experimental Therapeutics

EVOLUTION OF THE AUTONOMIC INNERVATION OF VISCERAL AND CARDIOVASCULAR SYSTEMS IN VERTEBRATES

¹ Department of Zoology, University of Melbourne, Parkville 3052, Victoria, Australia

1) The anatomy of the autonomic nervous system in teleost fish, amphibia, reptiles, and birds is essentially similar to that seen in mammals. However, a sacral parasympathetic system is not present in teleost fish and urodele amphibians and is only rudimentary in anurans. In cyclostome fish there are no sympathetic chains or segmental sympathetic ganglia and in elasmobranchs there are series of paravertebral ganglia linked by a loose plexus of nerve bundles rather than a compact sympathetic chain, and grey rami are absent.

2) The vagal supply to visceral muscles such as the stomach and lung is primitively nonadrenergic and inhibitory. At some evolutionary stage higher than the Amphibia, the cholinergic excitatory function classically attributed to the vagus has been transferred from the sympathetic to the parasympathetic outflow. This may also be correlated with the switch from primitive sympathetic cholinergic excitatory supply of the viscera to predominantly adrenergic inhibitory control.

3) The primitive parasympathetic innervation of the heart is cholinergic and inhibitory and this has been consistently retained throughout vertebrate evolution. Similarly adrenergic cardioaccelerator fibres appear early in evolution and are retained throughout. Primitively they run together with vagal fibres in the vagosympathetic trunks and only at the reptile level reach the heart by separate nerve trunks, although the presence of a few adrenergic fibres of sympathetic origin still remain in the vagal trunks even in mammals. The presence of special catecholamine-containing cells appears to be a consistent feature of the vertebrate heart.

4) Nerve trunks of the morphologically defined sympathetic nervous system in fish and amphibia consist of predominantly excitatory cholinergic fibres. There are various proportions of adrenergic and cholinergic fibres in sympathetic trunks in reptiles and birds, while in mammals, most, and sometimes all, of the fibres in sympathetic trunks are adrenergic. Thus, there has been an overall trend from cholinergic to adrenergic sympathetic control of visceral and vascular systems.

5) The development of preganglionic adrenergic fibres modulating the activity of nonadrenergic intramural ganglion cells in such organs as gut and bladder is not established until the mammals, although there is some rudimentary development of this kind in reptiles and birds.

6) The presence of intramural adrenergic nerve cells in various organs appears to be an evolutionary development that has taken place independently in many groups (e.g., lizard gut, toad lung, frog bladder). However it has not become established as a major feature of later evolution in mammals; no adrenergic cell bodies have been found in the gut and few in the heart and bladder.

7) The influence of circulating catecholamines released from diffusely clistributed chromaffin cells appears to play a much more significant role in lower, than in higher vertebrates, in which direct nervous control has been developed to a more sophisticated degree. Chromaffin tissue is widespread in cyclostomes and is closely associated with the segmentally arranged sympathetic ganglia in elasmobranchs and to a large extent in teleosts and amphibians.

8) Models have been put forward in this review of the pattern of evolution of the autonomic innervation of various visceral and cardiovascular systems. However it should be emphasised that these models are largely speculative and it is hoped that they will provoke further experimentation in the field which will lead to modification, refutation, and, one hopes, even support of some of the ideas proposed.

Note:

This work has been supported by Grants from the Australian Research Grants Committee and the National Heart Foundation of Australia. I am grateful to Eva Lederer, Bron Robinson, and Ann Dabscheck for their help in preparing the manuscript and to my colleagues John Furness, Terry Bennett, Graeme Campbell, John McLean, Mike Rand, Marion McCulloch, and Cohn Raper for their constructive criticisms.

This article has been cited by other articles:

				E. W. Taylor, D. V. Andrade, A. S. Abe, C. A. C. Leite, and T. Wang The unequal influences of the left and right vagi on the control of the heart and pulmonary artery in the rattlesnake, Crotalus durissus J. Exp. Biol., January 1, 2009; 212(1): 145 - 151. [Abstract] [Full Text] [PDF]

				G. Burnstock Physiology and Pathophysiology of Purinergic Neurotransmission Physiol Rev, April 1, 2007; 87(2): 659 - 797. [Abstract] [Full Text] [PDF]

				E. W. Taylor, D. Jordan, and J. H. Coote Central Control of the Cardiovascular and Respiratory Systems and Their Interactions in Vertebrates Physiol Rev, July 1, 1999; 79(3): 855 - 916. [Abstract] [Full Text] [PDF]

				X. F. Deng, S. Mulay, S. Chemtob, and D. R. Varma Mechanisms of the Atrium-Specific Positive Inotropic Activities of Quinidine- and Atropine-Like Agents in Rats J. Pharmacol. Exp. Ther., April 1, 1997; 281(1): 322 - 329. [Abstract] [Full Text]

				M. E. Schwab, R. Heumann, and H. Thoenen Communication between Target Organs and Nerve Cells: Retrograde Axonal Transport and Site of Action of Nerve Growth Factor Cold Spring Harb Symp Quant Biol, January 1, 1982; 46(0): 125 - 134. [Abstract] [PDF]

				R Bunge, M Johnson, and C. Ross Nature and nurture in development of the autonomic neuron Science, March 31, 1978; 199(4336): 1409 - 1416. [Abstract] [PDF]