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Immunohistochemical localization of serotonin, leu-enkephalin, tyrosine hydroxylase, and substance P within the visceral sensory area of cartilaginous fish

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Summary

We examined the distribution of immunoreactivity to serotonin (5-HT), leu-enkephalin (LENK), tyrosine-hydroxylase (TH), and substance P (SP) within the primary visceral sensory region of cartilaginous fish. Two genera of sharks, Squalus and Heterodontus, a skate, Raja, a ray, Myliobatis, and a holocephalian, Hydrolagus, were used. Cranial nerves, VII, IX, and X enter the visceral sensory complex from the lateral aspect and divide it into lobes. Based on sagittally cut sections, there are four lobes in Hydrolagus and five in Squalus, corresponding to the number of gill arches. The neurochemicals are differentially distributed within each lobe. LENK+ and 5-HT+fibers are located in all regions within the visceral sensory complex. SP+fibers are extremely dense in a dorsolateral subdivision and do not extend as far ventrally as 5-HT+ and LENK+fibers. The lobes lack 5-HT+cells, but contain a few LENK+ and SP+cells. Many TH+cells are distributed in dorsomedial portions of the complex, but there are few TH+fibers. Thus, the visceral sensory area of cartilaginous fish contains several divisions that can be distinguished by their neurochemical content.

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References

  • Altschuler SM, Bao X, Bieger D, Hopkins DA, Miselis RR (1989) Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 283:248–268

    Google Scholar 

  • Ariëns Kappers CU, Huber GC, Crosby EC (1936) The comparative anatomy of the nervous system of vertebrates, including man. Macmillan, New York

    Google Scholar 

  • Barrett DJ, Taylor EW (1985) Spontaneous efferent activity in branches of the vagus nerve controlling heart rate and ventilation in the dogfish. J Exp Biol 117:433–448

    Google Scholar 

  • Barry MA (1987) Central connections of the IXth, Xth, and XIth cranial nerves in the clearnose skate, Raja eglanteria. Brain Res 425:159–166

    Google Scholar 

  • Brauth SE, Reiner A, Kitt CA, Karten HJ (1983) The substance P-containing striato-tegmental path in reptiles: an immunohistochemical study. J Comp Neurol 219:305–327

    Google Scholar 

  • Carroll RL (1988) Vertebrate paleontology and evolution. Freeman, New York

    Google Scholar 

  • Ciriello J, Calaresu FR (1981) Projections from buffer nerves to the nucleus of the solitary tract: an anatomical and electrophysiological study in the cat. J Autonon Nerv Syst 3:299–310

    Google Scholar 

  • Compagno LJV (1973) Interrelationships of living elasmobranchs. In: Greenwood PH, Miles RS, Patterson C (eds) Interrelationships of fishes. Academic Press for the Linnean Society of London, London, pp 15–61

    Google Scholar 

  • Compagno LJV (1977) Phyletic relationships of living sharks and rays. Am Zool 17:303–322

    Google Scholar 

  • Daniel JF (1934) The elasmobranch fishes, 3rd edn. University of California Press, Berkeley, Calif

    Google Scholar 

  • Euler C von Hayward JN, Marttila I Wyman RJ (1973) Respiratory neurons of the ventrolateral nucleus of the solitary tract of cat: vagal input, spinal connections, and morphological identification. Brain Res 61:1–22

    Google Scholar 

  • Finger TE (1978) Gustatory pathways in the bullhead catfish. II. Facial lobe connections. J Comp Neurol 180:691–705

    Google Scholar 

  • Finger TE (1981) Enkephalin-like immunoreactivity in the gustatory lobes and visceral nuclei in the brains of the goldfish and catfish. Neuroscience 12:2747–2758

    Google Scholar 

  • Finger TE (1984) Vagotomy induced changes in acetyl cholinesterase staining and substance P-like immunoreactivity in the gustatory lobes of goldfish. Anat Embryol 170:257–264

    Google Scholar 

  • Gardiner SM, Bennett T (1989) Brain neuropeptides: actions on central cardiovascular control mechanisms. Brain Res Rev 14:79–116

    Google Scholar 

  • Gillis RA, Holke CJ, Hamilton BL, Norman WP, Jacobowitz DM (1980) Evidence that substance P is a neurotransmitter of baroand chemoreceptor afferents in nucleus tractus, solitarius. Brain Res 181:476–481

    Google Scholar 

  • Hart JL (1973) Pacific fishes, of Canada. Bulletin 180, fisheries research board of Canada. Canadian Government Publishing Centre Ottawa

    Google Scholar 

  • Helke CJ, Hill KM (1988) Immunohistochemical study of neuropeptides in vagal and glossopharyngeal afferent neurons in the rat. Neuroscience 26:539–551

    Google Scholar 

  • Helke CJ, O'Donohue TL, Jacobowitz DM (1980) Substance P as a baro- and chemoreceptor afferent neurotransmitter: immunocytochemical and neurochemical evidence in the rat. Peptides 1:1–9

    Google Scholar 

  • Henry JL Sessle BJ (1985) Effects of glutamate, substance P and eledoisin-related peptide in solitary tract neurones involved in respiration and respiratory reflexes. Neuroscience 14:863–873

    Google Scholar 

  • Higgins GA, Hoffman GE, Wray S, Schwaber JS (1984) Distribution of neurotensin-immunoreactivity within baroreceptive portions of the nucleus of the tractus solitarius and the dorsal vagal nucleus of the rat. J Comp Neurol 226:155–164

    Google Scholar 

  • Hökfelt T, Johansson O, Terenius L, Stein L (1977) The distribution of enkephalin-immunoreactive cell bodies in the rat central nervous system. Neurosci Lett 5:25–31

    Google Scholar 

  • Hökfelt T, Mårtensson R, Björklund A, Kleinau S, Goldstein M (1984) Distributional maps of tyrosine hydroxylase-immunoreactive neurons in the rat brain. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy, vol 2: Classical transmitters in the CNS, part 1. Elsevier, Amsterdam, pp 277–379

    Google Scholar 

  • Jessell TM (1983) Nociception. In: Krieger DT, Brownstein MJ, Martin JB (eds) Brain peptides. Wiley, New York, pp 315–332

    Google Scholar 

  • Kalia M, Sullivan JM (1982) Brainstem projections of sensory and motor components of the vagus nerve in the rat. J Comp Neurol 211:248–265

    Google Scholar 

  • Kalia M, Füxe K, Hökfelt T, Johansson O, Lang R, Ganten D, Cuello C, Terenius L (1984) Distribution of neuropeptide immunoreactive nerve terminals within the subnuclei of the nucleus of the tractus solitarius of the rat. J Comp Neurol 222:409–444

    Google Scholar 

  • Kalia M, Füxe K, Goldstein M (1985) Rat medulla oblongata. III. Adrenergic (C1 and C2) neurons, nerve fibers and presumptive terminal processes. J Comp Neurol 233:333–349

    Google Scholar 

  • Katz DM, Karten HJ (1983) Visceral representation within the nucleus of the tractus solitarius in the pigeon, Columba livia. J Comp Neurol 218:42–73

    Google Scholar 

  • Kawano H, Chiba T (1984) Distribution of substance P immunoreactive nerve terminals within the nucleus tractus solitarius of the rat. Neurosci Lett 45:175–179

    Google Scholar 

  • Kubota Y, Takagi H, Morishima Y, Powell JF, Smith AD (1985) Synaptic interaction between catecholaminergic neurons and substance P-immunoreactive axons in the caudal part of the nucleus of the solitary tract of the rat: demonstration by the electron microscopic mirror technique Brain Res 333:188–192

    Google Scholar 

  • Lee HS, Basbaum AI (1984) Immunoreactive pro-enkephalin and pro-dynorphin products are differently distributed within the nucleus of the solitary tract of the rat J Comp Neurol 230:614–619

    Google Scholar 

  • Leslie RA (1985) Neuroactive substances in the dorsal vagal complex of the medulla oblongata: nucleus of the tractus solitarius, area postrema, and dorsal motor nucleus of the vagus. Neurochem Int 7:191–211

    Google Scholar 

  • Mahoney G, Hillman DE, Canaday M (1990) High-resolution, large-area image recording and analysis. In: Toga AW (ed) Three-dimensional neuroimaging. Raven Press, New York, pp 73–86

    Google Scholar 

  • Maisey JG (1984) Higher elasmobranch phylogeny and biostratigraphy. Zool J Linn Soc 82:33–54

    Google Scholar 

  • Maley B, Elde R (1982) Immunohistochemical localization of putative neurotransmitters within the feline nucleus tractus solitarii. Neuroscience 7:2469–2490

    Google Scholar 

  • Maley B, Mullett T Elde R (1983) The nucleus tractus solitarii of the cat: a comparison of Golgi impregnated neurons with methionine-enkephalin- and substance P-immunoreactive neurons. J Comp Neurol 217:405–417

    Google Scholar 

  • Maley BE, Newton BW, Howes KA, Herman LM Oloff CM, Smith KC, Elde RP (1987) Immunohistochemical localization of substance P and enkephalin in the nucleus tractus solitarii of the rhesus monkey, Macaca mulatta. J Comp Neurol 260:483–490

    Google Scholar 

  • Manaker S, Verderame HM (1990) Organization of serotonin 1A and 1B receptors in the nucleus of the solitary tract. J Comp Neurol 301:535–553

    Google Scholar 

  • Morilak DA, Morris M, Chalmers J (1988) Release of substance P in the nucleus tractus solitarius measured by in vivo microdialysis: response to stimulation of the aortic depressor nerves in rabbit. Neurosci Lett 94:131–137

    Google Scholar 

  • Morin-Surun MP, Jordan D, Champagnat J, Spyer KM, Denavit-Saubie M (1984) Excitatory effects of iontophoretically applied substance P on neurons in the nucleus tractus, solitarius of the cat: lack of interaction with opiates and opioids. Brain Res 307:388–392

    Google Scholar 

  • Morita Y, Finger, TE (1985) Reflex connections of the facial and vagal gustatory systems in the brainstem of the bullhead catfish, Ictalurus nebulosus. J Comp Neurol 231:547–558

    Google Scholar 

  • Morita Y, Finger TE (1987) Topographic representation of the sensory and motor roots of the vagus nerve in the medulla of goldfish, Carassius auratus. J Comp Neurol 264:231–249

    Google Scholar 

  • Naik DR, Sar M, Stumpf WE (1981) Immunohistochemical localization of enkephalin in the central nervous system and pituitary of the lizard, Anolis carolinensis. J Comp Neurol 198:583–601

    Google Scholar 

  • Nelson JS (1984) Fishes of the world. Wiley, New York

    Google Scholar 

  • Norgren R (1978) Projections from the nucleus of the solitary tract in the rat. Neuroscience 3:207–218

    Google Scholar 

  • Northcutt RG (1989) Brain variation and phylogenetic trends in elasmobranch fishes. J Exp Zool [Suppl] 2:83–100

    Google Scholar 

  • Pickel VM, Joh TH, Chan J, Beaudet A (1984) Serotoninergic terminals: ultrastructure and synaptic interaction with catecholamine-containing neurons in the medial nuclei of the solitary tracts. J Comp Neurol 225:291–301

    Google Scholar 

  • Reiner A (1987) The distribution of proenkephalin-derived peptides in the central nervous system of turles. J Comp Neurol 259:65–91

    Google Scholar 

  • Reiner A, Northcutt RG (1987) An immunohistochemical study of the telencephalon of the African lungfish, Protopterus annectens. J Comp Neurol 256:463–481

    Google Scholar 

  • Reiner PB Vincent SR (1986) The distribution of tyrosine hydroxylase, dopamine-β-hydroxylase, and phenylethanolamine-N-methyltransferase immunoreactive neurons in the feline medulla oblongata. J Comp Neurol 248:518–531

    Google Scholar 

  • Reiner A, Karten HJ (1982) Enkephalin-mediated basal ganglia influences over the optic, tectum: immunohistochemistry of the tectum and the lateral spiriform nucleus in pigeon. J Comp Neurol 208:37–53

    Google Scholar 

  • Riche D, De Pommery J, Menetrey D (1990) Neuropeptides and catecholamines in efferent projections of the nuclei of the solitary tract in the rat. J Comp Neurol 293:399–424

    Google Scholar 

  • Seiders EP, Stuesse SL (1984) A horseradish peroxidase investigation of carotid sinus nerve components in the rat. Neurosci Lett 46:13–18

    Google Scholar 

  • Shapiro RE, Miselis RR (1985) The central organization of the vagus nerve innervating the stomach of the rat. J Comp Neurol 238:473–488

    Google Scholar 

  • Smeets WJAJ, Nieuwenhuys R (1976) Topological analysis of the brain stem of the sharks Squalus acanthias and Scyliorhinus canicula. J Comp Neurol 165:333–368

    Google Scholar 

  • Smeets WJAJ, Nieuwenhuys R, Roberts BL (1983) The central nervous system of cartilaginous fishes: structure and functional correlations. Springer, New York

    Google Scholar 

  • Stuesse SL, Cruce WLR (1991) Immunohistochemical localization of serotoninergic, enkephalinergic, and catecholaminergic cells in the brainstem of a cartilaginous fish, Hydrolagus colliei. J Comp Neurol 309:535–548

    Google Scholar 

  • Stuesse SL, Cruce WLR (1992) Distribution of tyrosine hydroxylase, serotonin, and leu-enkephalin immunoreactive cells in the brainstem of a shark, Squalus acanthias. Brain Behav Evol 39:77–92

    Google Scholar 

  • Stuesse SL, Cruce WLR, Northcutt RG (1990) Distribution of tyrosine hydroxylase and serotonin immunoreactivity in the central nervous system of the thornback guitarfish, Platyrhinoidis triseriata. J Chem Neuroanat 3:45–58

    Google Scholar 

  • Stuesse SL, Cruce WLR, Northcutt RG (1991a) Serotoninergic and enkephalinergic cell, groups in the reticular formation of the bat ray and two skates. Brain Behav Evol 38:39–52

    Google Scholar 

  • Stuesse SL, Cruce WLR, Northcutt RG (1991b) Localization of serotonin, tyrosine hydroxylase, and leu-enkephalin immunoreactive cells in the brainstem of the horn shark, Heterodontus francisci. J Comp Neurol 308:277–292

    Google Scholar 

  • Voorn P, Buijs RM (1983) An immuno-electronmicroscopical study comparing vasopressin, oxytocin, substance P and enkephalin containing nerve terminals, in the nucleus of the solitary tract of the rat. Brain Res 270:169–173

    Google Scholar 

  • Wild JM (1981) Identification and localization of the motor nuclei and sensory projections of the glossopharyngeal, vagus, and hypoglossal nerves of the cockatoo (Cacatua roseicapilla), Cacatuidac. J Comp Neurol 203:351–377

    Google Scholar 

  • Withington-Wray DJ, Roberts BL, Taylor EW (1986) The topographical organization of the vagal motor column in the elasmobranch fish, Scyliorhinus canicula L. J Comp Neurol 248:95–104

    Google Scholar 

  • Wolters JG, Donkelaar HJ ten, Verhofstad AA (1986) Distribution of some peptides (substance P, [Leu]enkephalin, [Met]enkephalin) in the brain stem and spinal cord of a lizard, Varanus exanthematicus. Neuroscience 18:917–946

    Google Scholar 

  • Yamanaka S, Honma Y, Ueda S, Sano Y (1990) Immunohistochemical demonstration of serotonin neuron system in the central nervous system of the Japanese dogfish, Scyliorhinus torazame (Chondrichthyes). J Hirnforsch 31:385–397

    Google Scholar 

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  1. Neurobiology Department Northeastern Ohio Universities College of Medicine, 4209 S.R. 44, 44272, Rootstown, OH, USA

    Sherry L. Stuesse, David C. Stuesse & William L. R. Cruce

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  1. Sherry L. Stuesse
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  2. David C. Stuesse
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Stuesse, S.L., Stuesse, D.C. & Cruce, W.L.R. Immunohistochemical localization of serotonin, leu-enkephalin, tyrosine hydroxylase, and substance P within the visceral sensory area of cartilaginous fish. Cell Tissue Res 268, 305–316 (1992). https://doi.org/10.1007/BF00318799

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