Autonomic Neuroscience: Basic and Clinical 165 (2011) 3–9 Contents lists available at ScienceDirect Autonomic Neuroscience: Basic and Clinical journal homepage: www.elsevier.com/locate/autneu Review Comparative anatomy of the autonomic nervous system Stefan Nilsson Department of Zoophysiology, Zoological Institute, University of Gothenburg, Box 463, SE 405 30 Göteborg, Sweden article info abstract Article history: This short review aims to point out the general anatomical features of the autonomic nervous systems of Received 4 January 2010 non-mammalian vertebrates. In addition it attempts to outline the similarities and also the increased Received in revised form 16 March 2010 complexity of the autonomic nervous patterns from fish to tetrapods. With the possible exception of the Accepted 26 March 2010 cyclostomes, perhaps the most striking feature of the vertebrate autonomic nervous system is the similarity between the vertebrate classes. An evolution of the complexity of the system can be seen, with the Keywords: segmental ganglia of elasmobranchs incompletely connected longitudinally, while well developed paired Autonomic nervous system Cranial nerve sympathetic chains are present in teleosts and the tetrapods. In some groups the sympathetic chains may be Enteric nervous system reduced (dipnoans and caecilians), and have yet to be properly described in snakes. Parasympathetic nervous system Cranial autonomic pathways are present in the oculomotor (III) and vagus (X) nerves of gnathostome fish Sympathetic nervous system and the tetrapods, and with the evolution of salivary and lachrymal glands in the tetrapods, also in the facial Vagus nerve (VII) and glossopharyngeal (IX) nerves. © 2010 Elsevier B.V. All rights reserved. Contents 1. Introduction ............................................................... 3 2. A note on the terminology ........................................................ 4 3. Arrangement of the autonomic nervous system in the different vertebrate groups . ............................. 4 4. Cyclostomes ............................................................... 5 5. Elasmobranchs .............................................................. 5 6. Teleosts ................................................................. 6 7. Dipnoans ................................................................ 6 8. Amphibians ............................................................... 7 9. Reptiles ................................................................. 7 10. Birds .................................................................. 8 11. Conclusions ............................................................... 8 Acknowledgments ............................................................... 8 References ................................................................... 8 1. Introduction complexity, and in differentiation, is most likely reflected in the physiology of these systems. One note of caution: anatomical, and for An autonomic nervous system, as originally defined by Langley that matter functional, studies that are used to provide a generalised (1898, 1921) is present in all vertebrates, although the anatomical representation of the autonomic innervation patterns in a certain arrangement in cyclostomes (lampetroids and myxinoids) is not well vertebrate group are limited to a very small number of species. Keeping understood. Starting from the elasmobranchs (sharks, rays and this in mind, it may still be possible to gain an overview of the evolution chimaeroids) and via teleosts (bony fish), amphibians and reptiles, it of the autonomic nervous system within the vertebrate kingdom. is at least possible to construct an image of the increased complexity of Useful, and more comprehensive, accounts of anatomical features the autonomic system along the vertebrate lineage. This increase in of the vertebrate autonomic system can be found in Nicol (1952), Burnstock (1969) and Nilsson (1983), who also includes functional aspects, and especially so in the comprehensive review by Gibbins E-mail address: [email protected]. (1994). There are numerous articles that present anatomical 1566-0702/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.autneu.2010.03.018 4 S. Nilsson / Autonomic Neuroscience: Basic and Clinical 165 (2011) 3–9 information from the different vertebrate classes (e.g., Gabella, 1976 of the parasympathetic pathways released acetylcholine as transmit- (mammals); Bennett, 1974 and Bolton, 1971 (birds); Taxi, 1976 ter substance, while those of the sympathetic system released (amphibians); Berger and Burnstock, 1979 (reptiles); Young, 1931, adrenaline or noradrenaline. These observations seemed to further 1933 (fish); and Nilsson and Holmgren, 1992 and Nilsson, in press strengthen the original anatomical terminology proposed by Langley, (dipnoans)). but later studies clearly demonstrate the lack of any parallel functional The aim of this brief outline is to provide a comparative overview of base for the terminology (e.g. Campbell, 1970). It may therefore be the autonomic nervous anatomy in the non-mammalian vertebrates. useful to, yet again, point out that the sometimes used terminology “sympathetic nerve=adrenergic nerve” mixes anatomical and func- 2. A note on the terminology tional facts in an infelicitous manner. When John Newport Langley proposed the term “autonomic nervous system” in 1898, he divided the system into three portions. 3. Arrangement of the autonomic nervous system in the different These came to be called (1) the sympathetic system, (2) the vertebrate groups parasympathetic system (“the allied nervous system of the cranial and sacral nerves”, and (3) the enteric system (“for the local nervous In all vertebrate classes, with the exception of the cyclostomes, a system of the gut”)(Langley 1898, 1921). This original subdivision, remarkably common pattern of the arrangement of the autonomic where the sympathetic systems are anatomically defined by pathways system is found. In the tetrapods, cranial autonomic pathways run leaving the spinal cord in the thoracic and lumbar regions, works well with cranial nerves III, VII, IX and X, although the presence of such for mammals (and, perhaps, for anuran amphibians). However, to pathways in the VII and IX cranial nerves of amphibians has been make the distinction between the posterior sympathetic and the debated (see later). In teleosts, elasmobranchs and dipnoans, cranial sacral parasympathetic pathways is difficult or even impossible in autonomic pathways occur in cranial nerves III and X, and in some of the non-mammalian species. A modified terminology was elasmobranchs there are some claims that also cranial nerves VII proposed by Nilsson (1983), where “cranial autonomic” is used to and IX include autonomic pathways — possibly with vasomotor describe the parasympathetic pathways running in the cranial nerves, function in the head (Nicol, 1952). and “spinal autonomic” is used for all sympathetic and sacral Interconnected paravertebral ganglia form a pair of well developed parasympathetic pathways as defined by Langley. The enteric system sympathetic chains in teleosts and all tetrapods. In dipnoans, retains its original label, but note that here the distinction between sympathetic chains are also present, albeit quite rudimentarily motor neurons (autonomic), sensory neurons and interneurons is (Giacomini, 1906). In elasmobranchs the segmental paravertebral often unclear (Furness and Costa, 1980) (see also contribution on ANS ganglia do not form continuous longitudinally connected chains, and gut motility by Olsson and Holmgren, this volume). although the general function appears to be similar to the other In the early days of research into the autonomic nervous system, groups (Young, 1933; Nicol, 1952). There are no sympathetic chains in there appeared to be some evidence that the postganglionic neurons the cyclostomes (Nicol, 1952; Fänge et al., 1963). Fig. 1. A simplified view of the organisation of the autonomic nervous system of an elasmobranch. Legend: an, anastomosis between spinal autonomic (sympathetic) and cranial nerves; ant spl n, anterior splanchnic nerve; ceph sc, cephalic sympathetic chain; cil g, ciliary ganglion; coel g, coeliac ganglion; comm., commisure between left and right sympathetic chain; deep ceph symp, deep cephalic sympathetic; deep cerv symp, deep cervical sympathetic; g imp, ganglion impar; hypo n, hypogastric nerve; inf mes g, inferior mesenteric ganglion; mid spl n, middle splanchnic nerve; nod g, nodose (vagal) ganglion; pet g, petrous (glossopharyngeal) ganglion; post spl nn, posterior splanchnic nerves; r comm, ramus communicans; sph g, sphenopalatine ganglion; sub g, submadibular ganglion; sup ceph symp, superior cephalic sympathetic; sup cerv g, superior cervical ganglion; sup cerv symp, superior cervical sympathetic; sup mes g, superior mesenteric ganglion; stell g, stellate ganglion; Roman numbers refer to the cranial nerves. Reproduced from Nilsson (1983) Autonomic nerve function in the vertebrates, Zoophysiology series, Vol. 13, Fig. 2.6, p.18, Springer-Verlag, Berlin, Heidelberg, New York. With kind permission of Springer Science+Business Media. S. Nilsson / Autonomic Neuroscience: Basic and Clinical 165 (2011) 3–9 5 4. Cyclostomes There is some difference between the two cyclostome groups, myxinoids and lampetroids, in the autonomic nerve arrangement. Cranial autonomic pathways in myxinoids occur only in the vagus (X), where a prominent innervation of the gall