Development of the serotoninergic system in the central nervous system of a shark, the lesser spotted dogfish Scyliorhinus canicula

Chondrychthyans (cartilaginous fishes) are key to understanding the ancestral gnathostome condition since they provide an outgroup to sarcopterygians and actinopterygians. To gain comparative knowledge about the development of the vertebrate serotoninergic systems, we studied by immunohistochemistry the origin, spatiotemporal organization, and migration patterns of serotonin‐containing neurons and the growth of axonal pathways in the central nervous system of a shark, the lesser spotted dogfish. Hindbrain serotonin‐immunoreactive cells arose close to the floor plate and most populations migrated ventrally and mediolaterally to form the various raphe and reticular groups. The order of appearance of serotoninergic populations in the rhombencephalon and spinal cord (first the superior groups and then the inferior and spinal populations) roughly matched with that reported in other vertebrates but important differences were noted in the formation of prosencephalic groups in fishes. In addition to preoptic and hypothalamic areas, serotoninergic cerebrospinal fluid‐contacting cells were observed in the isthmus (raphe dorsalis anterioris). Transient serotonin‐immunoreactive cells were noted in the pineal organ, habenula, and pretectum. Further, we provide a revised anatomical framework for reticular and raphe serotoninergic populations considering their origin and segmental organization. Two distinct phases of development of the serotoninergic innervation were distinguished, that of the formation of the main axonal pathways and that of the branching of fibers. The development of main serotoninergic ascending pathways in dogfish was notably similar to that described in mammals. Our findings suggest the conservation of developmental patterns in serotoninergic systems and enhance the importance of elasmobranchs for understanding the early evolution of this system in vertebrates. J. Comp. Neurol. 511:804–831, 2008. © 2008 Wiley‐Liss, Inc.

[1]  R. Anadón,et al.  Early development of GABAergic cells of the retina in sharks: An immunohistochemical study with GABA and GAD antibodies , 2008, Journal of Chemical Neuroanatomy.

[2]  R. Anadón,et al.  The segmental organization of the developing shark brain based on neurochemical markers, with special attention to the prosencephalon , 2008, Brain Research Bulletin.

[3]  R. Anadón,et al.  Tangentially migrating GABAergic cells of subpallial origin invade massively the pallium in developing sharks , 2008, Brain Research Bulletin.

[4]  H. Kung,et al.  Study of the spinal cords of the sturgeon Acipenser schrenckii, gar Lepisosteus oculatus, and goldfish Carassius auratus by morphological, immunohistochemical, and biochemical approaches , 2007, Microscopy research and technique.

[5]  R. Anadón,et al.  New Insights on Saccus vasculosus Evolution: A Developmental and Immunohistochemical Study in Elasmobranchs , 2007, Brain, Behavior and Evolution.

[6]  E. Kremmer,et al.  The serotonergic phenotype is acquired by converging genetic mechanisms within the zebrafish central nervous system , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[7]  E. Petrova,et al.  Serotonin is involved in the regulation of histogenetic processes in rat embryonic neocortex , 2007, Bulletin of Experimental Biology and Medicine.

[8]  A. Chiba Serotonergic neuron system in the spinal cord of the gar Lepisosteus oculatus (Lepisosteiformes, Osteichthyes) with special regard to the juxtameningeal serotonergic plexus as a paracrine site , 2007, Neuroscience Letters.

[9]  R. Anadón,et al.  Development of the serotonergic system in the central nervous system of the sea lamprey , 2006, International Journal of Developmental Neuroscience.

[10]  C. A. Byrd,et al.  Mitral cells in the olfactory bulb of adult zebrafish (Danio rerio): Morphology and distribution , 2006, The Journal of comparative neurology.

[11]  R. Dubuc,et al.  Ontogeny of 5‐HT neurons in the brainstem of the lamprey, Petromyzon marinus , 2006, The Journal of comparative neurology.

[12]  H. Yoshioka,et al.  Characterization and expression of serotonin transporter genes in zebrafish. , 2006, The Tohoku journal of experimental medicine.

[13]  R. Anadón,et al.  GABAergic system of the pineal organ of an elasmobranch (Scyliorhinus canicula): a developmental immunocytochemical study , 2006, Cell and Tissue Research.

[14]  J. Royet,et al.  5-hydroxytryptamine action in the rat olfactory bulb: In vitro electrophysiological patch-clamp recordings of juxtaglomerular and mitral cells , 2005, Neuroscience.

[15]  P. Branchereau,et al.  Ontogenic Changes of the Spinal GABAergic Cell Population Are Controlled by the Serotonin (5-HT) System: Implication of 5-HT1 Receptor Family , 2005, The Journal of Neuroscience.

[16]  R. Anadón,et al.  Temporal and spatial organization of tyrosine hydroxylase-immunoreactive cell groups in the embryonic brain of an elasmobranch, the lesser-spotted dogfish Scyliorhinus canicula , 2005, Brain Research Bulletin.

[17]  M. Bosma,et al.  Midline serotonergic neurones contribute to widespread synchronized activity in embryonic mouse hindbrain , 2005, The Journal of physiology.

[18]  E. Debski,et al.  Serotonergic reticular formation cells in Rana pipiens: Categorization, development, and tectal projections , 2005, The Journal of comparative neurology.

[19]  W. Walkowiak,et al.  Hodological characterization of the septum in anuran amphibians: I. Afferent connections , 2005, The Journal of comparative neurology.

[20]  R. Anadón,et al.  An experimental study of the connections of the telencephalon in the rainbow trout (Oncorhynchus mykiss). I: Olfactory bulb and ventral area , 2004, The Journal of comparative neurology.

[21]  R. Anadón,et al.  Experimental study of the connections of the telencephalon in the rainbow trout (Oncorhynchus mykiss). II: Dorsal area and preoptic region , 2004, The Journal of comparative neurology.

[22]  J. Fetcho,et al.  Ontogeny and innervation patterns of dopaminergic, noradrenergic, and serotonergic neurons in larval zebrafish , 2004, The Journal of comparative neurology.

[23]  J. Fetcho,et al.  Relationship of tyrosine hydroxylase and serotonin immunoreactivity to sensorimotor circuitry in larval zebrafish , 2004, The Journal of comparative neurology.

[24]  R. Anadón,et al.  Distribution and development of glutamic acid decarboxylase immunoreactivity in the spinal cord of the dogfish Scyliorhinus canicula (elasmobranchs) , 2004, The Journal of comparative neurology.

[25]  S. Wilson,et al.  Hedgehog and Fgf signaling pathways regulate the development of tphR-expressing serotonergic raphe neurons in zebrafish embryos. , 2004, Journal of neurobiology.

[26]  M. Wullimann,et al.  Connections of the ventral telencephalon (subpallium) in the zebrafish (Danio rerio) , 2004, Brain Research.

[27]  P. Gaspar,et al.  The developmental role of serotonin: news from mouse molecular genetics , 2003, Nature Reviews Neuroscience.

[28]  T. Sauka-Spengler,et al.  Characterization of Brachyury genes in the dogfish S. canicula and the lamprey L. fluviatilis. Insights into gastrulation in a chondrichthyan. , 2003, Developmental biology.

[29]  Luis Puelles,et al.  Forebrain gene expression domains and the evolving prosomeric model , 2003, Trends in Neurosciences.

[30]  R. Anadón,et al.  Development of catecholaminergic systems in the spinal cord of the dogfish Scyliorhinus canicula (Elasmobranchs). , 2003, Brain research. Developmental brain research.

[31]  R. Northcutt,et al.  Connections of the Pallial Telencephalon in the Senegal Bichir, Polypterus , 2003, Brain, Behavior and Evolution.

[32]  D. Jaillard,et al.  Structure and expression of three Emx genes in the dogfish Scyliorhinus canicula: functional and evolutionary implications. , 2002, Developmental biology.

[33]  B. Baratte,et al.  Pax6 expression patterns in Lampetra fluviatilis and Scyliorhinus canicula embryos suggest highly conserved roles in the early regionalization of the vertebrate brain , 2002, Brain Research Bulletin.

[34]  T. Sauka-Spengler,et al.  Structure and expression of an Otx5-related gene in the dogfish Scyliorhinus canicula: evidence for a conserved role of Otx5 and Crx genes in the specification of photoreceptors , 2001, Development Genes and Evolution.

[35]  S. Jo,et al.  Distribution of Serotonin Immunoreactivitiy in the Main Olfactory Bulb of the Mongolian Gerbil , 2001, Anatomia, histologia, embryologia.

[36]  R. Anadón,et al.  A DiI-tracing study of the neural connections of the pineal organ in two elasmobranchs (Scyliorhinus canicula and Raja montagui) suggests a pineal projection to the midbrain GnRH-immunoreactive nucleus , 2001, Cell and Tissue Research.

[37]  W. Smeets,et al.  Catecholamine systems in the brain of vertebrates: new perspectives through a comparative approach , 2000, Brain Research Reviews.

[38]  S. Kuratani,et al.  Developmental Morphology of Branchiomeric Nerves in a Cat Shark, Scyliorhinus torazame, with Special Reference to Rhombomeres, Cephalic Mesoderm, and Distribution Patterns of Cephalic Crest Cells , 2000 .

[39]  R. Anadón,et al.  Distribution of choline acetyltransferase immunoreactivity in the brain of an elasmobranch, the lesser spotted dogfish (Scyliorhinus canicula) , 2000, The Journal of comparative neurology.

[40]  W. Smeets,et al.  Evolution of the basal ganglia: new perspectives through a comparative approach , 2000, Journal of anatomy.

[41]  J. Muñoz-Cueto,et al.  Distribution of serotonin in the brain of the Senegalese sole, Solea senegalensis: an immunohistochemical study , 2000, Journal of Chemical Neuroanatomy.

[42]  R. Anadón,et al.  Distribution of serotonin (5HT)‐immunoreactive structures in the central nervous system of two chondrostean species (Acipenser baeri and Huso huso) , 1999, The Journal of comparative neurology.

[43]  A. Chiba,et al.  Serotonin-immunoreactive structures in the central nervous system of the garfish Lepisosteus productus (Semionotiformes, Osteichthyes) , 1999, Neuroscience Letters.

[44]  R. Anadón,et al.  Afferent and efferent connections of the parapineal organ in lampreys: A tract tracing and immunocytochemical study , 1999, The Journal of comparative neurology.

[45]  O. Marín,et al.  Cholinergic and GABAergic neuronal elements in the pineal organ of lampreys, and tract-tracing observations of differential connections of pinealofugal neurons , 1999, Cell and Tissue Research.

[46]  A. Martínez-Marcos,et al.  Septal complex of the telencephalon of lizards: III. Efferent connections and general discussion , 1998, The Journal of comparative neurology.

[47]  A. Martínez-Marcos,et al.  Identification of the reptilian basolateral amygdala: an anatomical investigation of the afferents to the posterior dorsal ventricular ridge of the lizard Podarcis hispanica , 1998, The European journal of neuroscience.

[48]  W. Smeets,et al.  Basal ganglia organization in amphibians: Chemoarchitecture , 1998, The Journal of comparative neurology.

[49]  J. Nicholls,et al.  Three‐dimensional visualization of the distribution, growth, and regeneration of monoaminergic neurons in whole mounts of immature mammalian CNS , 1998, The Journal of comparative neurology.

[50]  J. Dubbeldam,et al.  Organization and efferent connections of the archistriatum of the mallard, Anas platyrhynchos L.: An anterograde and retrograde tracing study , 1997, The Journal of comparative neurology.

[51]  A. Martínez-Marcos,et al.  Septal complex of the telencephalon of the lizard Podarcis hispanica. II. afferent connections , 1997, The Journal of comparative neurology.

[52]  W. Smeets,et al.  Distribution of choline acetyltransferase immunoreactivity in the brain of anuran (Rana perezi, Xenopus laevis) and urodele (Pleurodeles waltl) amphibians , 1997, The Journal of comparative neurology.

[53]  W. Smeets,et al.  Basal ganglia organization in amphibians: Afferent connections to the striatum and the nucleus accumbens , 1997, The Journal of comparative neurology.

[54]  R. Tsien,et al.  Multiple Structural Elements in Voltage-Dependent Ca2+ Channels Support Their Inhibition by G Proteins , 1996, Neuron.

[55]  P. Gaspar,et al.  Transient Uptake and Storage of Serotonin in Developing Thalamic Neurons , 1996, Neuron.

[56]  J. Wild,et al.  Organization of afferent and efferent projections of the nucleus basalis prosencephali in a passerine, Taeniopygia guttata , 1996, The Journal of comparative neurology.

[57]  M. Druse,et al.  Serotonin as a developmental signal , 1995, Behavioural Brain Research.

[58]  W. Cruce,et al.  Raphe nuclei in three cartilaginous fishes, Hydrolagus colliei, Heterodontus francisci, and Squalus acanthias , 1995, The Journal of comparative neurology.

[59]  P. Ekström,et al.  Hypophysiotrophic systems in the brain of the Atlantic salmon. Neuronal innervation of the pituitary and the origin of pituitary dopamine and nonapeptides identified by means of combined carbocyanine tract tracing and immunocytochemistry , 1995, Journal of Chemical Neuroanatomy.

[60]  P. Ekström Developmental changes in the brain-stem serotonergic nuclei of teleost fish and neural plasticity , 1994, Cellular and Molecular Neurobiology.

[61]  M. Herbin,et al.  Organization of the serotoninergic system in the brain of two amphibian species, Ambystoma mexicanum (Urodela) and Typhlonectes compressicauda (Gymnophiona) , 1994, Anatomy and Embryology.

[62]  A. Reiner,et al.  Distribution of choline acetyltransferase immunoreactivity in the pigeon brain , 1994, The Journal of comparative neurology.

[63]  H. Künzle,et al.  Connections of the basal telencephalic areas c and d in the turtle brain , 1994, Anatomy and Embryology.

[64]  S. Grillner,et al.  5‐HT innervation of reticulospinal neurons and other brainstem structures in lamprey , 1994, The Journal of comparative neurology.

[65]  M. A. Ali,et al.  Development of serotonergic neurons in the brain of the mackerel, Scomber scombrus. An immunohistochemical study , 1994 .

[66]  K. Sillar,et al.  Descending serotonergic spinal projections and modulation of locomotor rhythmicity in Rana temporaria embryos , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[67]  L. P. Morin,et al.  Development of the hamster serotoninergic system: Cell groups and diencephalic projections , 1993, The Journal of comparative neurology.

[68]  J. Mellinger,et al.  A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish (Chondrichthyes: Scyliorhinidae) , 1993 .

[69]  Luis Puelles,et al.  Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization , 1993, Trends in Neurosciences.

[70]  R. Sullivan,et al.  Serotonergic influence on olfactory learning in the neonate rat. , 1993, Behavioral and neural biology.

[71]  J. Lauder,et al.  Neurotransmitters as growth regulatory signals: role of receptors and second messengers , 1993, Trends in Neurosciences.

[72]  W. Smeets,et al.  Distribution of choline acetyltransferase immunoreactivity in the brain of the lizard Gallotia galloti , 1993, The Journal of comparative neurology.

[73]  N. Okado,et al.  Development of serotoninergic system in the brain and spinal cord of the chick , 1992, Progress in Neurobiology.

[74]  L. Ebbesson,et al.  Transient serotonin-immunoreactive neurons coincide with a critical period of neural development in coho salmon (Oncorhynchus kisutch) , 1992, Cell and Tissue Research.

[75]  N. Vesselkin,et al.  The serotoninergic system of the brain of the lamprey, Lampetra fluviatilis: an evolutionary perspective , 1992, Journal of Chemical Neuroanatomy.

[76]  T. Kadota Distribution of 5-HT (serotonin) immunoreactivity in the central nervous system of the inshore hagfish,Eptatretus burgeri , 1991, Cell and Tissue Research.

[77]  W. Cruce,et al.  Immunohistochemical localization of serotoninergic, enkephalinergic, and catecholaminergic cells in the brainstem and diencephalon of a cartilaginous fish, hydrolagus colliei , 1991, The Journal of comparative neurology.

[78]  R. Northcutt,et al.  Localization of serotonin, tyrosine hydroxylase, and leu‐enkephalin immunoreactive cells in the brainstem of the horn shark, Heterodontus francisci , 1991, The Journal of comparative neurology.

[79]  H. Korf,et al.  Immunocytochemical localization of serotonin and photoreceptor-specific proteins (rod-opsin, S-antigen) in the pineal complex of the river lamprey, Lampetra japonica, with special reference to photoneuroendocrine cells , 1990, Cell and Tissue Research.

[80]  E. Rodríguez,et al.  The paraventricular and posterior recess organs of elasmobranchs: A system of cerebrospinal fluid-contacting neurons containing immunoreactive serotonin and somatostatin , 1990, Cell and Tissue Research.

[81]  J. Lauder Ontogeny of the Serotonergic System in the Rat: Serotonin as a Developmental Signal a , 1990, Annals of the New York Academy of Sciences.

[82]  H. Meissl,et al.  Electron microscopic analysis of S‐antigen‐ and serotonin‐immuoreactive neural and sensory elements in the photosensory pineal organ of the salmon , 1990, The Journal of comparative neurology.

[83]  S. Ebbesson,et al.  Distribution of serotonin-immunoreactive neurons in the brain of sockeye salmon fry. , 1989, Journal of chemical neuroanatomy.

[84]  R. Keynes,et al.  Segmental patterns of neuronal development in the chick hindbrain , 1989, Nature.

[85]  H. Karten,et al.  Immunohistochemical study of the telencephalon of the spiny dogfish, Squalus acanthias , 1988, The Journal of comparative neurology.

[86]  S. Ebbesson,et al.  The left habenular nucleus contains a discrete serotonin-immunoreactive subnucleus in the coho salmon (Oncorhynchus kisutch) , 1988, Neuroscience Letters.

[87]  E Fiebig,et al.  Connections of the corpus cerebelli in the thornback guitarfish, Platyrhinoidis triseriata (Elasmobranchii): A study with WGA‐HRP and extracellular granule cell recording , 1988, The Journal of comparative neurology.

[88]  H. Joosten,et al.  The development of serotonergic raphespinal projections in Xenopus laevis , 1986, International Journal of Developmental Neuroscience.

[89]  N. Okado,et al.  Immunohistochemical study on the development of serotoninergic neurons in the chick: II. Distribution of cell bodies and fibers in the spinal cord , 1986, The Journal of comparative neurology.

[90]  S. Grillner,et al.  A spinal projection of 5-hydroxytryptamine neurons in the lamprey brainstem; evidence from combined retrograde tracing and immunohistochemistry , 1986, Neuroscience Letters.

[91]  J. Wallace An immunocytochemical study of the development of central serotoninergic neurons in the chick embryo , 1985, The Journal of comparative neurology.

[92]  T. van Veen,et al.  Distribution of 5‐hydroxytryptamine (serotonin) in the brain of the teleost Gasterosteus aculeatus L. , 1984, The Journal of comparative neurology.

[93]  M. Geffard,et al.  Immunocytochemical localization and circadian variations of serotonin and N-acetylserotonin in photoreceptor cells. Light and electron microscopic study in the teleost pineal organ. , 1984, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[94]  D. McAdoo,et al.  The distribution of serotonin in the CNS of an elasmobranch fish: Immunocytochemical and biochemical studies in the atlantic stingray, Dasyatis sabina , 1983, The Journal of comparative neurology.

[95]  J. Lauder,et al.  Development of the serotonergic system in the rat embryo: An immunocytochemical study , 1983, Brain Research Bulletin.

[96]  M. Molliver,et al.  Immunohistochemical study of the development of serotonergic neurons in the rat CNS , 1982, Brain Research Bulletin.

[97]  T. Ritchie,et al.  Immunocytochemical demonstration of serotonergic cells, terminals and axons in the spinal cord of the stingray, dasyatis sabina , 1982, Brain Research.

[98]  M. Molliver,et al.  An immunohistochemical study of serotonin neuron development in the rat: Ascending pathways and terminal fields , 1982, Brain Research Bulletin.

[99]  W. Smeets,et al.  Cells of origin of pathways descending to the spinal cord in two chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata , 1981, The Journal of comparative neurology.

[100]  W. Saidel,et al.  Forebrain connections in the goldfish support telencephalic homologies with land vertebrates. , 1981, Science.

[101]  T. Veen,et al.  The pineal complex of the three-spined stickleback, Gasterosteus aculeatus L. , 1980, Cell and Tissue Research.

[102]  B. Kedrowsky Die Stoffaufnahme bei Opalina ranarum. Mitteilung V. Der Segregationsapparat , 1931, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[103]  L. Nyberg,et al.  Serotonin and opsin immunoreactivities in the developing pineal organ of the three-spined stickleback, Gasterosteus aculeatus L. , 2004, Cell and Tissue Research.

[104]  M. Schreibman,et al.  Immunocytochemical localization of serotonin in the brain and pituitary gland of the platyfish, Xiphophorus maculatus , 2004, Cell and Tissue Research.

[105]  R. van Kesteren,et al.  The Role of Neurotransmitters in Neurite Outgrowth and Synapse Formation , 2003, Reviews in the neurosciences.

[106]  L. Bally-Cuif,et al.  Cloning of two tryptophan hydroxylase genes expressed in the diencephalon of the developing zebrafish brain. , 2002, Gene expression patterns : GEP.

[107]  W. Smeets,et al.  Basal ganglia organization in amphibians: efferent connections of the striatum and the nucleus accumbens. , 1997, The Journal of comparative neurology.

[108]  S. Grillner,et al.  Rostrocaudal distribution of 5-HT innervation in the lamprey spinal cord and differential effects of 5-HT on fictive locomotion. , 1996, The Journal of comparative neurology.

[109]  A. Reiner,et al.  Neurotransmitter organization and connectivity of the basal ganglia in vertebrates: implications for the evolution of basal ganglia. , 1995, Brain, behavior and evolution.

[110]  R. Baker,et al.  Conservation of neuroepithelial and mesodermal segments in the embryonic vertebrate head. , 1993, Acta anatomica.

[111]  M. Schreibman,et al.  Hypophysiotropic neurons in the hypothalamus of the catfish Clarias batrachus: a cobaltous lysine and HRP study. , 1993, Brain, behavior and evolution.

[112]  M. A. Ali,et al.  Immunohistochemical study of the development of serotoninergic neurons in the brain of the brook trout Salvelinus fontinalis. , 1992, Brain, behavior and evolution.

[113]  W. Cruce,et al.  Distribution of tyrosine hydroxylase, serotonin, and leu-enkephalin immunoreactive cells in the brainstem of a shark, Squalus acanthias. , 1992, Brain, behavior and evolution.

[114]  R. Northcutt,et al.  Afferent and efferent connections of the bullfrog medial pallium. , 1992, Brain, behavior and evolution.

[115]  D. H. Paul,et al.  Brainstem neurons projecting to different levels of the spinal cord of the dogfish Scyliorhinus canicula. , 1992, Brain, behavior and evolution.

[116]  R. Northcutt,et al.  Serotoninergic and enkephalinergic cell groups in the reticular formation of the bat ray and two skates. , 1991, Brain, behavior and evolution.

[117]  S. Ueda,et al.  Immunohistochemical demonstration of serotonin neuron system in the central nervous system of the Japanese dogfish, Scyliorhinus torazame (Chondrichthyes). , 1990, Journal fur Hirnforschung.

[118]  R. Northcutt,et al.  Distribution of tyrosine hydroxylase- and serotonin-immunoreactive cells in the central nervous system of the thornback guitarfish, Platyrhinoidis triseriata. , 1990, Journal of chemical neuroanatomy.

[119]  Northcutt Rg,et al.  Medullary and Mesencephalic Pathways and Connections of Lateral Line Neurons of the Spiny Dogfish Squalus acanthias , 1988 .

[120]  R. L. Boord,et al.  Medullary and mesencephalic pathways and connections of lateral line neurons of the spiny dogfish Squalus acanthias. , 1988, Brain, behavior and evolution.

[121]  J. Collin,et al.  Indoles in the photoreceptor cells of the lamprey pineal complex. , 1986, Annales d'endocrinologie.

[122]  N. Okado,et al.  Immunohistochemical study on the development of serotoninergic neurons in the chick: I. Distribution of cell bodies and fibers in the brain , 1986, The Journal of comparative neurology.

[123]  L. Nyberg,et al.  Ontogenetic development of serotoninergic neurons in the brain of a teleost, the three-spined stickleback. An immunohistochemical analysis. , 1985, Brain research.

[124]  W. Smeets,et al.  The central nervous system of cartilaginous fishes: a neuro-anatomical study based on normal and experimental material , 1983 .

[125]  W. Smeets Efferent tectal pathways in two chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata , 1981, The Journal of comparative neurology.