Cholinergic and nitrergic neuronal networks in the goldfish telencephalon

Acta Neurobiologiae Experimentalis

Volumn 73, Issue 3, 2013, Pages 338-353

  Giraldez Perez, Rosa María ^a   Gaytan, Susana Pilar ^a   Pasaro, Rosario ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Acetylcholine; Goldfish; Histochemistry; Immunohistochemistry; Nitric oxide; Telencephalon

Indexed keywords

CHOLINE ACETYLTRANSFERASE; NEURONAL NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANIMAL; ARTICLE; CHOLINERGIC NERVE CELL; CYTOLOGY; GOLDFISH; METABOLISM; NERVE CELL NETWORK; NITRERGIC NERVE; PHYSIOLOGY; TELENCEPHALON;

ANIMALS; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC NEURONS; GOLDFISH; NADPH DEHYDROGENASE; NERVE NET; NITRERGIC NEURONS; NITRIC OXIDE SYNTHASE TYPE I; TELENCEPHALON;

EID: 84885743622     PISSN: 00651400     EISSN: 16890035     Source Type: Journal    
DOI: None     Document Type: Article

References (75)

1. Adrio F, Anadón R, Rodríguez-Moldes I (2000) Distribution of choline acetyltransferase (ChAT) immunoreactivity in the central nervous system of a chondrostean, the siberian sturgeon (Acipenser baeri). J Comp Neurol 426: 602-621.
2. Alonso JR, Porteros A, Crespo C, Arévalo R, Briñón JG, Weruaga E, Aijón J (1998) Chemical anatomy of the macaque monkey olfactory bulb: NADPH-diaphorase/ nitric oxide synthase activity. J Comp Neurol 402: 419-434.
3. Anadón R, Molist P, Rodríguez-Moldes I, López JM, Quintela I, Cervino MC, Barja P, González A (2000) Distribution of choline acetyltransferase immunoreactivity in the brain of an elasmobranch, the lesser spotted dogfish (Scyliorhinus canicula). J Comp Neurol 420: 139-170.
4. Ando H, Shi Q, Kusakabe T, Ohya T, Suzuki N, Urano A (2004) Localization of mRNAs encoding alpha and beta subunits of soluble guanylyl cyclase in the brain of rainbow trout: comparison with the distribution of neuronal nitric oxide synthase. Brain Res 1013: 13-29.
5. Arévalo R, Alonso JR, García-Ojeda E, Briñón JG, Crespo C, Aijón J (1995) NADPH-diaphorase in the central nervous system of the tench (Tinca tinca L, 1758). J Comp Neurol 352: 398-420.
6. Bond CE, Zimmermann M, Greenfield SA (2009) Upregulation of alpha7 nicotinic receptors by acetylcholinesterase C-terminal peptides. PLoS One 4: e4846.
7. Bordieri L, Persichini T, Venturini G, Cioni C (2003) Expression of nitric oxide synthase in the preoptic-hypothalamo-hypophyseal system of the teleost Oreochromis niloticus. Brain Behav Evol 62: 43-55.
8. Braford MR Jr (2009) Stalking the everted telencephalon: comparisons of forebrain organization in basal ray-finned fishes and teleosts. Brain Behav Evol 74: 56-76.
9. Brantley RK, Bass AH (1988) Cholinergic neurons in the brain of a teleost fish (Porichthys notatus) located with a monoclonal antibody to choline acetyltransferase. J Comp Neurol 275: 87-105.
10. Breer H, Shepherd GM (1993) Implications of the NO/ cGMP system for olfaction. Trends Neurosci 16: 5-9.
11. Briñón JG, Alonso JR, García-Ojeda E, Arévalo R, Porteros A, Velasco A, Aijón J (1994) Parvalbumin immunoreactivity in the telencephalic hemispheres of the tench, Tinca tinca. Arch Ital Biol 132: 1-12.
12. Butcher LL (1995) Cholinergic neurons and networks. In: The Rat Nervous System, 2nd ed. (Paxinos G, Ed.). Academic Press, San Diego, CA, p. 1003-1015.
13. Castro A, Becerra M, Manso MJ, Anadón R (2003) Distribution and development of calretinin-like immunoreactivity in the telencephalon of the brown trout, Salmo trutta fario. J Comp Neurol 467: 254-269.
14. Castro A, Becerra M, Manso MJ, Anadón R (2006) Calretinin immunoreactivity in the brain of the zebrafish, Danio rerio: distribution and comparison with some neuropeptides and neurotransmitter-synthesizing enzymes. I. Olfactory organ and forebrain. J Comp Neurol 494: 435-459.
15. Clemente D, Porteros A, Weruaga E, Alonso JR, Arenzana FJ, Aijon J, Arévalo R (2004) Cholinergic elements in the zebrafish central nervous system: Histochemical and immunohistochemical analysis. J Comp Neurol 4742: 75-107.
16. Clemente D, Arenzana FJ, Sánchez-González R, Porteros A, Aijón J, Arévalo R (2005) Comparative analysis of the distribution of choline acetyltransferase in the central nervous system of cyprinids. Brain Res Bull 66: 546-549.
17. Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Snyder SH (1991) Nitric oxide syntase and neuronal NADPH diaphorase are identical in brain and peripheral tissue. Proc Natl Acad Sci U S A 88: 7797-7801.
18. Dellacorte C, Kalinoski DL, Huque T, Wysocki L, Restrepo D (1995) NADPH diaphorase staining suggests localization of nitric oxide synthase within mature vertebrate olfactory neurons. Neuroscience 66: 215-225.
19. Edwards JG, Greig A, Sakata Y, Elkin D, Michel WC (2007) Cholinergic innervation of the zebrafish olfactory bulb. J Comp Neurol 504: 631-645.
20. Ekström P (1987) Distribution of choline acetyltransferaseimmunoreactive neurons in the brain of a cyprinid teleost (Phoxinus phoxinus L.). J Comp Neurol 256: 494-515.
21. Folgueira M, Anadón R, Yáñez J (2004) Experimental study of the connections of the telencephalon in the rainbow trout (Oncorhynchus mykiss). II: Dorsal area and preoptic region. J Comp Neurol 480: 204-233.
22. Ganz J, Kaslin J, Freudenreich D, Machate A, Geffarth M, Brand M (2012) Subdivisions of the adult zebrafish subpallium by molecular marker analysis. J Comp Neurol 520: 633-655.
23. Giassi AC, Harvey-Girard E, Valsamis B, Maler L (2012) Organization of the gymnotiform fish pallium in relation to learning and memory: I. Cytoarchitectonics and cellular morphology. J Comp Neurol 520: 3314-3337.
24. Gilbert D, Lecchi M, Arnaudeau S, Bertrand D, Demaurex N (2009) Local and global calcium signals associated with the opening of neuronal alpha7 nicotinic acetylcholine receptors. Cell Calcium 45: 198-207.
25. Giraldez-Perez RM, Gaytan SP, Ruano D, Torres B, Pasaro R (2008) Distribution of NADPH-diaphorase and nitric oxide synthase reactivity in the central nervous system of the goldfish (Carassius auratus). J Chem Neuroanat 35: 12-32.
26. Giraldez-Perez RM, Gaytan SP, Torres B, Pasaro R (2009) Co-localization of nitric oxide synthase and choline acetyltransferase in the brain of the goldfish (Carassius auratus). J Chem Neuroanat 37: 1-17.
27. González A, Moreno N, López JM (2002) Distribution of NADPH-diaphorase/nitric oxide synthase in the brain of the caecilian Dermophis mexicanus (amphibia: gymnophiona): comparative aspects in amphibians, Brain Behav Evol 60: 80-100.
28. Guirado S, Real MA, Dávila JC (2008) Distinct immunohistochemically defined areas in the medial amygdala in the developing and adult mouse. Brain Res Bull 75: 214-217.
29. Harvey-Girard E, Giassi AC, Ellis W, Maler L (2012) Organization of the gymnotiform fish pallium in relation to learning and memory: IV. Expression of conserved transcription factors and implications for the evolution of dorsal telencephalon. J Comp Neurol. 520: 3395-3413.
30. Havekes R, Abel T, Van der Zee EA (2011) The cholinergic system and neostriatal memory functions. Behav Brain Res 221: 412-423.
31. Huang PL, Dawson TM, Bredt DS, Snyder SH, Fishman MC (1993) Targeted disruption of the neuronal nitric oxide synthase gene. Cell 75: 1273-1286.
32. Ichikawa T, Ajiki K, Matsuura J, Misawa H (1997) Localization of two cholinergic markers, choline acetyltransferase and vesicular acetylcholine transporter in the central nervous system of the rat: in situ hybridization histochemistry and immunohistochemistry. J Chem Neuroanat 13: 23-39.
33. Ito H, Yamamoto N (2009) Non-laminar cerebral cortex in teleost fishes? Biol Lett 5: 117-121.
34. Jadhao AG, Malz CR (2004) Nicotinamide adenine dinucleotide phosphate (NADPH)-diaphorase activity in the brain of a cichlid fish, with remarkable findings in the entopeduncular nucleus: a histochemical study. J Chem Neuroanat 27: 75-86.
35. Jadhao AG, Wilke I, Meyer DL (1999) NADPH-diaphorase expression in the hypothalamo-hypophysial system of different catfish. J Hirnforsch 39: 513-523.
36. Karnovsky MJ, Roots L (1964) A "direct-coloring" thiocholine method for cholinesterase. J Histochem Cytochem 12: 219-221.
37. Le Jeune H, Jourdan F (1994) Acetylcholinesterase-containing intrinsic neurons in the rat main olfactory bulb: cytological and neurochemical features. Eur J Neurosci 6: 1432-1444.
38. Lema SC, Nevitt GA (2001) Re-evaluating NADPH-diaphorase histochemistry as an indicator of nitric oxide synthase: an examination of the olfactory system of coho salmon (Oncorhynchus kisutch). Neurosci Lett 313: 1-4.
39. López JM, González A (2002) Ontogeny of NADPH diaphorase/nitric oxide synthase reactivity in the brain of Xenopus laevis. J Comp Neurol 445: 59-77.
40. López JM, Perlado J, Morona R, Northcutt RG, González A (2012) Neuroanatomical organization of the cholinergic system in the central nervous system of a basal actinopterygian fish, the Senegal bichir Polypterus senegalus. J Comp Neurol 521: 24-49.
41. MacLeod NK, Lowe GA (1976) Field potentials in the olfactory bulb of the rainbow trout (Salmo gairdneri): evidence for a dendrodendritic inhibitory pathway. Exp Brain Res 25: 255-266.
42. Marín O, Smeets WJ, González A (1997) Distribution of choline acetyltransferase immunoreactivity in the brain of anuran (Rana perezi, Xenopus laevis) and urodele (Pleurodeles waltl) amphibians. J Comp Neurol 382: 499-534.
43. Medina L, Reiner A (1994) Distribution of choline acetyltransferase immunoreactivity in the pigeon brain. J Comp Neurol 342: 497-537.
44. Medina L, Smeets WJ, Hoogland PV, Puelles L (1993) Distribution of choline acetyltransferase immunoreactivity in the brain of the lizard Gallotia galloti. J Comp Neurol 331: 261-285.
45. Meek J, Nieuwenhuys R (1998) Holosteans and teleosts. In: The Central Nervous System of Vertebrates. (Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C, Eds) Springer-Verlag, Berlin, DE, p. 759-937.
46. Mueller T, Wullimann MF (2009) An evolutionary interpretation of teleostean forebrain anatomy. Brain Behav Evol 74: 30-42.
47. Mueller T, Vernier P, Wullimann MF (2004) The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio. Brain Res 1011: 156-169.
48. Mueller T, Dong Z, Berberoglu MA, Guo S (2011) The dorsal pallium in zebrafish, Danio rerio (Cyprinidae, Teleostei). Brain Res 1381: 95-105.
49. Muñoz M, Muñoz A, Marín O, Alonso JR, Arévalo R, Porteros A, González A (1996) Topographical distribution of NADPH-diaphorase activity in the central nervous system of the frog, Rana perezi. J Comp Neurol 367: 54-69.
50. Murakami T, Morita Y, Ito H (1983) Extrinsic and intrinsic fiber connections of the telencephalon in a teleost, Sebastiscus marmoratus. J Comp Neurol 216: 115-131.
51. Nathan C, Xie QW (1994) Nitric oxide synthases: roles, tolls, and controls. Cell 78: 915-918.
52. Nickell WT, Shipley MT (1988) Two anatomically specific classes of candidate cholinoceptive neurons in the rat olfactory bulb. J Neurosci 8: 4482-4491.
53. Nieuwenhuys R (2009) The forebrain of actinopterygians revisited. Brain Behav Evol 73: 229-252.
54. Nieuwenhuys R (2011) The development and general morphology of the telencephalon of actinopterygian fishes: synopsis, documentation and commentary. Brain Struct Funct 215: 141-157.
55. Northcutt RG (2006) Connections of the lateral and medial divisions of the goldfish telencephalic pallium. J Comp Neurol 494: 903-943.
56. Northcutt RG (2008) Forebrain evolution in bony fishes. Brain Res Bull 75: 191-205.
57. Northcutt RG (2011) Do teleost fishes possess a homolog of mammalian isocortex? Brain Behav Evol 78: 136-138.
58. Paxinos G, Watson CR, Emson PC (1980) AChE-stained horizontal sections of the rat brain in stereotaxic coordinates. J Neurosci Methods 3: 129-149.
59. Pérez SE, Yánez J, Marín O, Anadón R, González A, Rodríguez-Moldes I (2000) Distribution of choline acetyltransferase (ChAT) immunoreactivity in the brain of the adult trout and tract-tracing observations on the connections of the nuclei of the isthmus. J Comp Neurol 428: 450-474.
60. Phelps PE, Houser CR, Vaughn JE (1992) Small cholinergic neurons within fields of cholinergic axons characterize olfactory-related regions of rat telencephalon. Neuroscience 48: 121-136.
61. Portavella M, Vargas JP (2005) Emotional and spatial learning in goldfish is dependent on different telencephalic pallial systems. Eur J Neurosci 21: 2800-2806.
62. Portavella M, Torres B, Salas C (2004a) Avoidance response in goldfish: emotional and temporal involvement of medial and lateral telencephalic pallium. J Neurosci 24: 2335-2342.
63. Portavella M, Torres B, Salas C, Papini MR (2004b) Lesions of the medial pallium, but not of the lateral pallium, disrupt spaced-trial avoidance learning in goldfish (Carassius auratus). Neurosci Lett 362: 75-78.
64. Rodríguez-Moldes I, Molist P, Adrio F, Pombal MA, Yañez SE, Mandado M, Marín O, López JM, González A, Anadón R (2002) Organization of cholinergic systems in the brain of different fish groups: a comparative analysis. Brain Res Bull 57: 331-334.
65. Salas C, Broglio C, Durán E, Gómez A, Ocaña FM, Jiménez-Moya F, Rodríguez F (2006) Neuropsychology of learning and memory in teleost fish. Zebrafish 3: 157-171.
66. Schober A, Malz CR, Schober W, Meyer DL (1994) NADPH-diaphorase in the central nervous system of the larval lamprey (Lampetra planeri). J Comp Neurol 345: 94-104.
67. Schoenfeld TA, Knott TK (2002) NADPH diaphorase activity in olfactory receptor neurons and their axons conforms to a rhinotopically-distinct dorsal zone of the hamster nasal cavity and main olfactory bulb. J Chem Neuroanat 24: 269-285.
68. Sims KL, Kauffman FC, Johnson EC, Pickel VM (1974) Cytochemical localization of brain nicotinamide adenine dinucleotide phosphate (oxidized)-dependent dehydrogenases Qualitative and quantitative distributions. J Histochem Cytochem 22: 7-19.
69. Singru PS, Sakharkar AJ, Subhedar N (2003) Neuronal nitric oxide synthase in the olfactory system of an adult teleost fish Oreochromis mossambicus. Brain Res 977: 157-168.
70. Suárez J, Dávila JC, Real MA, Guirado S, Medina L (2006) Calcium-binding proteins, neuronal nitric oxide synthase, and GABA help to distinguish different pallial areas in the developing and adult chicken. I. Hippocampal formation and hyperpallium. J Comp Neurol 497: 751-771.
71. Virgili M, Poli A, Beraudi A, Giuliani A, Villani L (2001) Regional distribution of nitric oxide synthase and NADPH-diaphorase activities in the central nervous system of teleosts. Brain Res 901: 202-207.
72. Wullimann MF, Rink E (2002) The teleostean forebrain: a comparative and developmental view based on early proliferation, Pax6 activity and catecholaminergic organization. Brain Res Bull 57: 363-370.
73. Wullimann MF, Mueller T (2004) Teleostean and mammalian forebrains contrasted: evidence from genes to behaviour. J Comp Neurol 475: 143-162.
74. Yamamoto N, Ishikawa Y, Yoshimoto M, Xue HG, Bahaxar N, Sawai N, Yang CY, Ozawa H, Ito H (2007) A new interpretation on the homology of the teleostean telencephalon based on hodology and a new eversion model. Brain Behav Evol 69: 96-104.
75. Yoshihara Y, Nagao H, Mori K (2001) Neurobiology. Sniffing out odors with multiple dendrites. Science 291: 835-837