Th e Central Nervous System of Lungfi shes

Th e central nervous system of lungfi shes consists of a spinal cord and brain. Th e spinal cord is cylindrical and is composed of a central canal, surrounded by a core of gray matter, surrounded, in turn, by white matter. Th e gray matter is divided into dorsal, lateral, medial, and ventrolateral cellular columns. Th e white matter consists of dorsal, lateral, and ventral funiculi, which comprise both ascending and descending axonal tracts. Th e South American lungfi sh, Lepidosiren paradoxa (Fitzinger 1837) and African lungfi shes, such as the Spotted African lungfi sh, Protopterus dolloi (Boulenger 1900) all have slender brains, with both the hindbrain and the telencephalic hemispheres being wider than the diencephalon and midbrain. Th e Australian lungfi sh, Neoceratodus forsteri (Krefft 1870) also has a slender brain, but the cerebellum and optic tectum are relatively larger than those structures in other lungfi shes. Although there is an extensive descriptive literature on the brain in each genus of lungfi shes, there are few immunohistochemical or hodological studies. Th e literature is reviewed, and the anatomy of the brain and spinal cord of the Spotted African lungfi sh is described in detail, beginning with the spinal cord and continuing rostrally through the telencephalon and olfactory bulbs. Th ere is general agreement on the basic anatomy of the hindbrain and midbrain in all three lungfi sh genera, but the organization of the forebrain is poorly understood and the subject of disagreement. Most of the controversy on its organization centers on diff ering interpretations of the pallial-subpallial border, the extent of the

striatopallidal systems, and the organization of the amygdala. Each of these areas of disagreement is reviewed, and a new model of telencephalic organization in lungfi shes is proposed. In this model, the telencephalon of lungfi shes is far more similar to that of amphibians than has previously been suspected. Th e chapter ends with a series of proposals concerning future directions for neurobiological research on these fi shes. Keywords: diencephalon, cerebellum, hindbrain, midbrain, prosencephalon, spinal cord

One or more parts of the central nervous system (CNS) have been described in each genus of lungfi shes by several researchers: 1) Lepidosiren (Elliot Smith 1908; Nieuwenhuys and Meek 1990; Zambrano and Iturriza 1972, 1973; Th ors and Nieuwenhuys 1979; Northcutt 1986a; Nieuwenhuys 1998); 2) Neoceratodus (Beauregard 1881; Sanders 1889; Wilder 1887; Bing and Burckhardt 1904, 1905; Holmgren and van der Horst 1925; Keenan 1928; Jeener 1930; Nieuwenhuys and Hickey 1965; Nieuwenhuys 1967a; von Bartheld et al. 1990; Nieuwenhuys and Meek 1990; Whitt 1969; Northcutt 1986a); and 3) Protopterus (Burckhardt 1892; Kölliker 1896; Jeener 1930; Gerlach 1933; Holmgren 1922, 1959; Rudebeck 1945, Dorn 1957; Schnitzlein 1966; Schnitzlein and Crosby 1967, 1968; Nieuwenhuys 1967a, b, 1969; Capanna and Clairambault 1973; Clairambault and Capanna 1973; Clairambault et al. 1974a, b, c; von Bartheld and Meyer 1988; von Bartheld 1992; von Bartheld et al. 1990; Northcutt 1986a, 2008). Th e descriptive neuroanatomy of the two genera of lepidosirenid lungfi shes (Lepidosiren and Protopterus) is far more complete than that of Neoceratodus. Th e most recent neuroanatomical description of the entire CNS of a lungfi sh is that for Lepidosiren (Nieuwenhuys 1998), and there is no recent description of the entire CNS of Neoceratodus or Protopterus. In order to partially rectify this problem, the CNS of the Spotted African lungfi sh, Protopterus dolloi Boulenger 1900, will be emphasized in this chapter. Although there is a fairly extensive descriptive literature on the CNS of lungfi shes, far less is known about the development or immunohistochemistry of the CNS in these fi shes. Bing and Burckhardt (1905) briefl y described the development of the brain of Neoceratodus and Whiting et al. (1992) described the development of the brain and cranial nerves. Rudebeck (1945) provided the most detailed description of the development of the telencephalon of Protopterus, whereas Bergquist (1932) undertook a similar description of the development of the diencephalon of Neoceratodus. Th us, there are no recent descriptions of the development of the entire brain or the expression of any of the genes involved in the development of the CNS of lungfi shes. Th ere are also few immunohistochemical studies of the CNS in lungfi shes. Reiner and Northcutt (1987) described the distribution of a number of neuroactive substances (substance P, leucine-enkephalin, avian pancreatic polypetid and

LANT6) in the forebrain of Protopterus annectens. Th e telencephalic distribution of acetylcholinesterase (AChE) in Neoceratodus and Protopterus was described by von Bartheld et al. (1990). Vallarino et al. (1992, 1995) described the distribution of α-melanocyte-stimulating hormone and neuropeptid Y, respectively in P. annectens. Th e distribution of the peptide FMRFamide in the terminal nerve fi bers of Neoceratodus has been described by Fiorentino et al. (2002). Finally, messenger RNAs encoding for two gutamic acid decarboxylases (GAD65 and GAD67) have been characterized in P. annectens and their distribution in the brain described by Trabucchi et al. (2008). Further, there are only a handful of experimental studies on the CNS in lungfi shes. Th e primary olfactory and terminal nerve projections in P. dolloi were described by von Bartheld and colleagues (von Bartheld and Meyer 1988; von Bartheld et al. 1988). Th e projections of the terminal nerve have also been described in Neoceratodus (Schober et al. 1994), as have the projections of the paraventricular organ in P. dolloi (von Bartheld and Meyer 1990). Th e retinal projections to the diencephalon and midbrain have been described in Lepidosiren (Northcutt 1977), in Neoceratodus (Northcutt 1980), and in Protopterus (Clairambault and Flood 1975; Northcutt 1977). Th e oculomotor and mesencephalic trigeminal neurons have been localized in Neoceratodus and Protopterus (von Bartheld, 1992). Finally, the central projections of the lateral line nerves in lepidosirenid lungfi shes (Northcutt 1983a) and the descending projections to the spinal cord in Protopterus (Ronan and Northcutt 1985) have been established. Th e gross brain structure of lungfi shes (Fig. 1) is reviewed and compared to the brains of other lobe-fi nned fi shes (Fig. 2). Th e major divisions of the brain (Figs. 3-10) and what is known about their connections are then described, beginning with the spinal cord and continuing rostrally through the telencephalon and olfactory bulbs. Finally, the chapter ends with a short section on future directions for neurobiological research on lungfi shes.