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Autonomic Neuroscience: Basic and Clinical 165 (2011) 3–9

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Autonomic Neuroscience: Basic and Clinical

journal homepage: www.elsevier.com/locate/autneu

Review Comparative of the

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 . 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 . With the possible exception of the Accepted 26 March 2010 cyclostomes, perhaps the most striking feature of the autonomic nervous system is the similarity between the vertebrate classes. An 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 reduced (dipnoans and caecilians), and have yet to be properly described in . 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 . Keeping understood. Starting from the elasmobranchs (, 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- (); 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 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, ; 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, ; 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 ; 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, ; 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 bladder has been demonstrated (Fänge and Johnels, 1958). In the lampetroids there may in addition run autonomic, probably vasomotor, nerves in the facial (VII) and glossopharyngeal (IX) nerve (Tretjakoff, 1927; Nicol, 1952). As mentioned earlier, there are no sympathetic chains in the cyclostomes, but scattered ganglia along the dorsal aorta may Fig. 2. Simplified summary of the anatomical arrangement of nerves in the region of the represent a spinal autonomic vasomotor innervation (Fänge et al., ciliary ganglion of mammals and teleost fish. In teleosts the profundus nerve is separate 1963). In the brook lamprey, Lampetra planeri, autonomic pathways from the trigeminal nerve and carries a ganglion (the profundus ganglion) separate from (and probably also somatic motor neurons) leave the spinal cord via the Gasserian ganglion. Legend: cil brev, ciliaris brevis (short ciliary nerve); cil g, ciliary ganglion; cil long, ciliaris longa (long ciliary nerve); Gass g, Gasserian ganglion of the both dorsal and ventral roots (Johnels, 1956; Campbell, 1970). trigeminal nerve; prof g, profundus ganglion; r brev, radix brevis (short ciliary root); r long, radix longa (long ciliary root); r symp, radix sympathica; symp, nerve fibres of spinal 5. Elasmobranchs autonomic (sympathetic) origin, i.e. fibres from superior cervical sympathetic ganglion () or fibres from the cephalic sympathetic chain (teleost); III, oculomotor nerve; Cranial autonomic pathways run in the oculomotor (III) and vagus V, trigeminal nerve. Reproduced from Nilsson (1983) Autonomic nerve function in the vertebrates, (X) nerves of elasmobranchs, and possibly also in the facial (VII) and Zoophysiology series, Vol. 13, Fig. 12.1, p.192, Springer-Verlag, Berlin, Heidelberg, New glossopharyngeal (IX) although the latter still needs further clarifi- York. With kind permission of Springer Science+Business Media. cation (Young, 1933; Nicol, 1952). The oculomotor pathways synapse in the ciliary ganglion and the postganglionic neurons control smooth muscle in the eye (Young, 1933). Vagal pathways run to the heart and gut, but the possible autonomic control of effectors in the gills remains With the exception, again, of the cyclostomes (see later) the unclear (Young, 1933)(Fig. 1). autonomic pathways leave the central nervous system via the ventral The paravertebral ganglia in elasmobranchs are segmentally roots of the spinal nerves. Dorsal root efferents have also been claimed arranged, but not completely connected longitudinally to form true for amphibians (Pick, 1970), but if such an arrangement exists, it is not sympathetic chains of the type seen in teleosts and the tetrapods. the rule (Campbell and Duxson, 1978; Nilsson, 1978). Preganglionic autonomic fibres leave the spinal cord in white

Fig. 3. A simplified view of the organisation of the autonomic nervous system of a teleost. Legend as in Fig. 1. Reproduced from Nilsson (1983) Autonomic nerve function in the vertebrates, Zoophysiology series, Vol. 13, Fig. 2.7, p. 21, Springer-Verlag, Berlin, Heidelberg, New York. With kind permission of Springer Science+Business Media. 6 S. Nilsson / Autonomic Neuroscience: Basic and Clinical 165 (2011) 3–9

(myelinated) rami communicantes, but there are no recurrent grey In the anterior end, a fine strand enters the posterior cardinal vein (unmyelinated) rami (Young, 1933). The largest chain ganglia are the (“azygos vein”) possibly innervating the chromaffin cells lining the most anterior pair known as axillary bodies. These bodies (called wall of this vein (Abrahamsson et al., 1979). “Axillar-Herz” by Leydig (1853)) are composed not only of postgan- glionic nerve cell bodies, but also large quantities of chromaffin cells, which presumably receive an innervation from preganglionic fibres (Young, 1933). An anterior splanchnic nerve leaves each axillary body, and fuse to a plexus along the coeliac artery. Segmental mid- and posterior splanchnic nerves leave the more posterior paravertebral ganglia. Also these ganglia comprise clusters of chromaffin cells. It should be noted that in contrast to the situation in mammals, the autonomic pathways running in the splanchnic nerves in fish are made up mainly, or even solely, of postganglionic fibres (Stannius, 1849; Young, 1933 Nicol, 1952). A summary of the general anatomical features of the elasmobranch autonomic nervous system is offered in Fig. 1.

6. Teleosts

Cranial autonomic pathways in teleosts are restricted to the oculomotor(III)andvagus(X)nerves.Asshownearlier,the oculomotor nerve sends fibres to the ciliary ganglion via the short ciliary root (radix brevis) and the eye is innervated by postganglionic fibres from the ciliary ganglion running in the short ciliary nerve. Vagal pathways are plentiful and give rise to branchial, cardiac and (gastro-)intestinal branches (see Nilsson, 1983). In teleosts, the sympathetic chains continue forward into the head, with in contact with several of the cranial nerves. A comparison between the arrangement of the sympathetic chains/nerves and the ciliary ganglion of the oculomotor nerve (III) in mammals and teleosts is shown in Fig. 2 (Nilsson, 1976, 1980). Connections between the two chains can occur along the length of the chains as in the stargazer Uranoscopus scaber (Young, 1931, or be restricted to a single connection at the level of the coeliac ganglion as in the Atlantic cod Gadus morhua (Nilsson, 1976). The coeliac ganglion is composed of the fused first trunk ganglia of the right chain, and is quite large in Gadus. The anterior splanchnic nerve is composed of postganglionic neurons, and runs from the coeliac ganglion to various viscera (see Fig. 3). At the level of the coeliac ganglion in Gadus, a small nerve runs to innervate the chromaffin tissue in the walls of the posterior cardinal veins (Nilsson, 1976). The innervations of the teleost swimbladder is quite complex, comprising a mixture of vagal and splanchnic pathways (Nilsson, 2009). Posteriorly, at the ganglion impar, the two sympathetic chains fuse to a single strand. At this level, a posterior splanchnic nerve emerges to innervate the urinogenital organs (Figs. 3 and 4; Young, 1931; Nilsson, 1976).

7. Dipnoans

Cranial autonomic pathways are restricted to the vagus (X) in the African (Protopterus sp.) and the South American lungfish (Lepidosiren paradoxa), but in the Australian lungfish (Neoceratodus forsteri), which possesses better developed eyes, there are also pathways in the Fig. 4. Simplified ventral view of the autonomic nervous system of a teleost, the cod Gadus oculomotor (III) nerve (Nicol, 1952). A vagal control of the lung and morhua. Legend: ant spl, anterior splanchnic nerve(s); cil g, ciliary ganglion; comm., heart has been shown, and it should be noted that the lungfish heart commisure between left and right sympathetic chains; in X, intestinal branch of the vagus stores large quantities of catecholamines in chromaffin cells within nerve; post spl, posterior splanchnic nerve (vesicular nerve); sat g, satellite ganglion; Roman numerals refer to the cranial nerves, while the Arabic numerals indicate the spinal the atrium (Abrahamsson et al., 1979; Scheuermann, 1979, 1993). A fi fi nerves. Asterisks indicate the sympathetic branches to the chromaf n tissue of the head vagal innervation of these chromaf n cells has been postulated kidney. Numerous branches from the sympathetic chains enter the cranial nerves, (Scheuermann, 1979). including the posterior parts of the intestinal branches of the vagi. At the level of the 20th Sympathetic chains were first described in lungfish by Giacomini pair of gangla, the posterior splanchnic nerve emerges to innervate the urinogenital (1906). The chains are delicate and poorly developed, but have been organs. The ganglion impar can be seen at the fusion of the left and right chain at the 21st pair of ganglia. described in both Protopterus and Lepidosiren. The chains form loops Reproduced from Holmgren S and Nilsson S (1982) Neuropharmacology of adrenergic (annuli) around the intercostal arteries, and may send pathways to neurons in teleost fish. Comp. Biochem. Physiol. 72C:289–302. With kind permission from the clusters of chromaffin cells that occur in the walls of these arteries. Elsevier. S. Nilsson / Autonomic Neuroscience: Basic and Clinical 165 (2011) 3–9 7

functional anatomy (histochemistry) and physiology/pharmacology of the autonomic control of various organs in anuran amphibians, notably the cane toad (Bufo marinus) (see, e.g., Burnstock, 1969; Campbell and Duxson, 1978). Understanding of the ANS of urodele amphibians is less complete, and that of apodan amphibians (caecilians) very limited, although the reduced sympathetic chain of these has been described (Norris and Hughes, 1918; Francis, 1934; Nicol, 1952). The cranial autonomic nervous system of amphibians runs in the oculomotor nerve to the eye (III), and definitely also in the vagus (X). Fibres in the facial (VII) and glossopharyngeal (IX) nerves have been debated, but control of the lachrymal and salivary glands may be present in the palatine branch of the facial nerve, and in the anterior branch of the glossopharyngeal. Vagal (X) pathways run to the anterior gut, lungs and heart (Nicol, 1952; Pick, 1970). Preganglionic pathways in both ventral and dorsal roots of the spinal nerves have been suggested for amphibians (Pick, 1970), although a dorsal root outflow appears to be questionable from many studies (Langley and Orbeli, 1911; Campbell and Duxson, 1978; Nilsson, 1978; see Fig. 5). Fibres from the anterior parts of the sympathetic chains enter the cranial nerves IX and X, forming mixed trunks. Such contributions may also exist to the V and VII cranial nerves, at least in some species, and there is also a contribution to the ciliary ganglion (Fig. 6). Fig. 5. Arrangement of the spinal autonomic (sympathetic) innervation of the spleen of the Chromaffin tissue occurs as ventral bands on the kidneys in frogs fl toad, Bufo marinus. Recordings on the right show the effect on ow through the perfused fi spleen in response to electrical stimulation of the ventral roots of spinal nerve 1–7on and toads, but in the urodeles chromaf ncellsoccurinthe perfusion flow through the toad spleen. Legend: cg, coeliac ganglion; pgsn, preganglionic sympathetic chain ganglia, resembling the arrangement in the splanchnic nerve. elasmobranchs (Nicol, 1952). Reproduced from Nilsson (1978) Sympathetic innervation of the spleen of the cane toad, – Bufo marinus. Comp. Biochem. Physiol. 61C:133 149. With kind permission from Elsevier. 9. Reptiles

The arrangement of the autonomic nervous system in reptiles is A simplified summary of the anatomy of the autonomic nervous very much like that of mammals, although functional information system in lungfish is offered by Nilsson and Holmgren (1992). (especially) would benefit from more studies. Cranial autonomic pathways have been demonstrated in cranial nerves III, VII, IX and X. It 8. Amphibians is perhaps noteworthy, that a description of sympathetic chains in snakes is wanting (for discussion, see Gibbins, 1994). The autonomic nervous system of amphibians has been well A general picture of the reptilian autonomic nervous system is elucidated ever since the early part of the 20th century. Work of the summarised in Fig. 7, and a good review is that of Berger and Melbourne group from the 1960s and 1970s helped understand the Burnstock (1979).

Fig. 6. A simplified view of the organisation of the autonomic nervous system of an amphibian. Legend as in Fig. 1. Reproduced from Nilsson (1983) Autonomic nerve function in the vertebrates, Zoophysiology series, Vol. 13, Fig. 2.8, p.24, Springer-Verlag, Berlin, Heidelberg, New York. With kind permission of Springer Science+Business Media. 8 S. Nilsson / Autonomic Neuroscience: Basic and Clinical 165 (2011) 3–9

Fig. 7. A simplified view of the organisation of the autonomic nervous system of a reptile. Legend as in Fig. 1. Reproduced from Nilsson (1983) Autonomic nerve function in the vertebrates, Zoophysiology series, Vol. 13, Fig. 2.10, p.27, Springer-Verlag, Berlin, Heidelberg, New York. With kind permission of Springer Science+Business Media.

10. Birds Swedish Research Council, VR (previously in the form of the Natural Science Research Council, NFR). The avian autonomic nervous system does not deviate much from that of the mammals, and the most notable differences would be References (1) that many postganglionic autonomic fibres do, indeed, carry a myelin sheath, (2) that the sympathetic chains are largely enclosed in Abrahamsson, T., Holmgren, S., Nilsson, S., Pettersson, K., 1979. On the chromaffin the vertebrae, and (3) the arrangement of the remarkable ganglion- system of the African lungfish, Protopterus aethiopicus. Acta Physiol. Scand. 107, 135–139. ated nerve of Remak. Remak's nerve, although not formally a part of Bennett, T., 1974. Peripheral and autonomic nervous system. In: Farner, D.S., King, J.S., the enteric nervous system, runs along the gut and is involved in its Parkes, K.C. (Eds.), Avian Biology 4. 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