The cholinergic system in the brain has been widely studied in most vertebrate groups, but there is no information available about this neurotransmission system in the brains of holostean fishes, a primitive and poorly understood group of actinopterygian fishes. The present study provides the first detailed information on the distribution of cholinergic cell bodies and fibers in the central nervous system in two holostean species, the Florida gar, Lepisosteus platyrhincus, and the bowfin, Amia calva. Immmunohistochemistry against the enzyme choline acetyltransferase (ChAT) revealed distinct groups of ChAT-immunoreactive (ChAT-ir) cells in the habenula, isthmic nucleus, laterodorsal tegmental nucleus, octavolateral area, reticular formation, cranial nerve motor nuclei and the motor column of the spinal cord, all of which seem to be highly conserved among vertebrates. Some ChAT-ir cells were detected in the basal telencephalon that appear in actinopterygians for the first time in the evolution of this neurotransmission system, whereas the remarkable cholinergic population in the optic tectum is a peculiar characteristic, the presence of which varies throughout evolution, although it is present in all teleosts studied. Abundant cholinergic fibers were found in the pretectal region and optic tectum, where they probably modulate vision, and in the hypothalamus and the interpeduncular neuropil. Some interspecific differences were also observed, such as the presence of ChAT-ir cells in the supraoptoparaventricular band only in Lepisosteus and in in the nucleus subglomerulosus only in Amia. In addition, ChAT-ir fibers in the olfactory bulb were detected only in Amia. Comparison of these results with those from other classes of vertebrates, and a segmental analysis to correlate cell populations, reveal that the pattern of the cholinergic system in holosteans is very close to that in ancestral actinopterygian fishes, as recently described in the bichir (Cladistia), although an important evolutionary novelty in holosteans is the presence of cholinergic cells in the basal telencephalon.

1.
Adams JC (1981): Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem 29:775.
2.
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.
3.
Aizawa H, Bianco IH, Hamaoka T, Miyashita T, Uemura O, Concha ML, Russell C, Wilson SW, Okamoto H (2005): Laterotopic representation of left-right information onto the dorso-ventral axis of a zebrafish midbrain target nucleus. Curr Biol 15:238-243.
4.
Alonso JR, Amaral DG (1995): Cholinergic innervation of the primate hippocampal formation. I. Distribution of choline acetyltransferase immunoreactivity in the Macaca fascicularis and Macaca mulatta monkeys. J Comp Neurol 355:135-170.
5.
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.
6.
Armstrong DM, Rotler A, Hersh LB, Pickel VM (1988): Localization of choline acetyltransferase in perikarya and dendrites within the nuclei of the solitary tracts. J Neurosci Res 20:279-290.
7.
Armstrong DM, Saper CB, Levey AI, Wainer H, Terry R (1983): Distribution of cholinergic neurons in rat brain: demostrated by the immunocytochemical localization of choline acetyltransferase. J Comp Neurol 216:53-68.
8.
Aroca P, Puelles L (2005): Postulated boundaries and differential fate in the developing rostral hindbrain. Brain Res Brain Res Rev 49:179-190.
9.
Bagnoli P, Fontanesi G, Alesci R, Erichsen JT (1992): Distribution of neuropeptide Y, substance P, and choline acetyltransferase in the developing visual system of the pigeon and effects of unilateral retina removal. J Comp Neurol 318:392-414.
10.
Baker BI, Bird DJ (2002): Neuronal organization of the melanin-concentrating hormone system in primitive actinopterygians: evolutionary changes leading to teleosts. J Comp Neurol 442:99-114.
11.
Bardet SM, Martínez-de-la-Torre M, Northcutt RG, Rubenstein JL, Puelles L (2008): Conserved pattern of OTP-positive cells in the paraventricular nucleus and other hypothalamic sites of tetrapods. Brain Res Bull 75:231-235.
12.
Beninato M, Spencer RF (1986): A cholinergic projection to the rat superior colliculus demonstrated by retrograde transport of horseradish peroxidase and choline acetyltransferase immunohistochemistry. J Comp Neurol 253:525-538.
13.
Bester H, Besson JM, Bernard JF (1997): Organization of efferent projections from the parabrachial area to the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol 383:245-281.
14.
Bhagwandin A, Fuxe K, Manger PR (2006): Choline acetyltransferase immunoreactive cortical interneurons do not occur in all rodents: a study of the phylogenetic occurrence of this neural characteristic. J Chem Neuroanat 32:208-216.
15.
Bianco IH, Wilson SW (2009): The habenular nuclei: a conserved asymmetric relay station in the vertebrate brain. Philos Trans R Soc Lond B Biol Sci 364:1005-1020.
16.
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.
17.
Brauth SE, Kitt CA, Price DL, Wainer BH (1985): Cholinergic neurons in the telencephalon of the reptile Caiman crocodilus. Neurosci Lett 58:235-240.
18.
Bulfone A, Puelles L, Porteus MH, Frohman MA, Martin GR, Rubenstein JL (1993): Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J Neurosci 13:3155-3172.
19.
Butcher LL, Woolf NJ (2004): Cholinergic neurons and networks revisited; in Paxinos GW (ed): The rat Central Nervous System. San Diego, Elsevier, pp 1257-1268.
20.
Butler AB, Northcutt RG (1982): Retinal projections in the bowfin Amia calva: cytoarchitectonic and experimental analysis. Brain Behav Evol 39:169-194.
21.
Cabrera B, Torres B, Pásaro R, Pastor AM, Delgado-García JM (1992): A morphological study of abducens nucleus motoneurons and internuclear neurons in the goldfish (Carassius auratus). Brain Res Bull 28:137-144.
22.
Cambronero F, Puelles L (2000): Rostrocaudal nuclear relationships in the avian medulla oblongata: a fate map with quail chick chimeras. J Comp Neurol 427:522-545.
23.
Castro A, Becerra M, Manso MJ, Anadón R (1999): Development of immunoreactivity to neuropepide Y in the brain of brown trout (Salmo trutta fario). J Comp Neurol 414:13-32.
24.
Chagnaud BP, Baker R, Bass AH (2011): Vocalization frequency and duration are coded in separate hindbrain nuclei. Nat Commun 2:346.
25.
Chandrasekhar A (2004): Turning heads: development of vertebrate branchiomotor neurons. Dev Dyn 229:143-161.
26.
Chiba A (2005): Neuropeptide Y-immunoreactive (NPY-ir) structures in the brain of the gar Lepisosteus oculatus (Lepisosteiformes, Oste-ichthyes) with special regard to their anatomical relations to gonadotropin-releasing hormone (GnRH)-ir structures in the hypothalamus and the terminal nerve. Gen Comp Endocrinol 142:336-346.
27.
Chiba A, Oka S (1999): Serotonin-immunoreactive structures in the central nervous system of the garfish Lepisosteus productus (Semionotiformes, Osteichthyes). Neurosci Lett 261:73-76.
28.
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.
29.
Clemente D, Porteros A, Weruaga E, Alonso JR, Arenzana FJ, Aijón J, Arévalo R (2004): Cholinergic elements in the zebrafish central nervous system: histochemical and immunohistochemical analysis. J Comp Neurol 474:75-107.
30.
Collin SP, Northcutt RG (1995): The visual system of the Florida garfish, Lepisosteus platyrhincus (Ginglymodi). IV. Bilateral projections and the binocular visual field. Brain Behav Evol 45:34-53.
31.
Concha ML, Wilson SW (2001): Asymmetry in the epithalamus of vertebrates. J Anat 199:63-84.
32.
Consonni S, Leone S, Becchetti A, Amadeo A (2009): Developmental and neurochemical features of cholinergic neurons in the murine cerebral cortex. BMC Neurosci 10:18.
33.
Crawford GD, Correa L, Salvaterra PM (1982): Interaction of monoclonal antibodies with mammalian choline acetyltransferase. Proc Natl Acad Sci USA 79:7031-7035.
34.
Desan PH, Gruberg ER, Grewell KM, Eckenstein F (1987): Cholinergic innervation of the optic tectum in the frog Rana pipiens. Brain Res 413:344-349.
35.
Díaz C, Yanes C, Trujillo CM, Puelles L (2000): Cytoarchitectonic subdivisions in the subtectal midbrain of the lizard Gallotia galloti. J Neurocytol 29:569-593.
36.
Eckenstein F, Thoenen H (1983): Cholinergic neurons in the rat cerebral cortex demonstrated by immunohistochemical localization of choline acetyltransferase. Neurosci Lett 36:211-215.
37.
Edwards JG, Greig A, Sakata Y, Elkin D, Michel WC (2007): Cholinergic innervation of the zebrafish olfactory bulb. J Comp Neurol 504:631-645.
38.
Ekström P (1987): Distribution of choline acetyltransferase-immunoreactive neurons in the brain of a cyprinid teleost (Phoxinus phoxinus L.). J Comp Neurol 256:494-515.
39.
Figdor MC, Stern CD (1993): Segmental organization of embryonic diencephalon. Nature 363:630-634.
40.
Folgueira M, Anadón R, Yáñez J (2004): An experimental study of the connections of the telencephalon in the rainbow trout (Oncorhynchus mykiss). I. Olfactory bulb and ventral area. J Comp Neurol 480:180-203.
41.
Fritzsch B (1998): Of mice and genes: evolution of vertebrate brain development. Brain Behav Evol 52:207-217.
42.
Gamse JT, Kuan YS, Macurak M, Brösamle C, Thisse B, Thisse C, Halpern ME (2005): Directional asymmetry of the zebrafish epithalamus guides dorsoventral innervation of the midbrain target. Development 132:4869-4881.
43.
Geula C, Schatz CR, Mesulam MM (1993): Differential localization of NADPH-diaphorase and calbindin-D28k within the cholinergic neurons of the basal forebrain, striatum and brainstem in the rat, monkey, baboon and human. Neuroscience 54:461-476.
44.
Gilland E, Baker R (1993): Conservation of neuroepithelial and mesodermal segments in the embryonic vertebrate head. Acta Anat (Basel) 148:110-123.
45.
Gilland E, Baker R (2005) Evolutionary patterns of cranial nerve efferent nuclei in vertebrates. Brain Behav Evol 66:234-254.
46.
Gillette MU, Mitchell JW (2002): Signaling in the suprachiasmatic nucleus: selectively responsive and integrative. Cell Tissue Res 309:99-107.
47.
Giráldez-Pérez 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.
48.
Goehler LE, Finger TE (1992): Functional organization of vagal reflex systems in the brain stem of the goldfish, Carassius auratus. J Comp Neurol 319:463-478.
49.
González A, López JM (2002): A forerunner of septohippocampal cholinergic system is present in amphibians. Neurosci Lett 327:111-114.
50.
González A, López JM, Sánchez-Camacho C, Marín O (2002): Localization of choline acetyltransferase (ChAT) immunoreactivity in the brain of a caecilian amphibian, Dermophis mexicanus (Amphibia: Gymnophiona). J Comp Neurol 448:249-267.
51.
González A, Meredith GE, Roberts BL (1993): Choline acetyltransferase immunoreactive neurons innervating labyrinthine and lateral line sense organs in amphibians. J Comp Neurol 332:258-268.
52.
González A, Northcutt RG (2009): An immunohistochemical approach to lungfish telencephalic organization. Brain Behav Evol 74:43-55.
53.
Graf W, Baker R (1985): The vestibuloocular reflex of the adult flatfish. I. Oculomotor organization. J Neurophysiol 54:887-899.
54.
Graf W, McGurk JF (1985): Peripheral and central oculomotor organization in the goldfish, Carassius auratus. J Comp Neurol 239:391-401.
55.
Gravett N, Bhagwandin A, Fuxe K, Manger PR (2009): Nuclear organization and morphology of cholinergic, putative catecholaminergic and serotonergic neurons in the brain of the rock hyrax, Procavia capensis. J Chem Neuroanat 38:57-74.
56.
Grover BG, Sharma SC (1981): Organization of extrinsic tectal connections in goldfish (Carassius auratus). J Comp Neurol 196:471-488.
57.
Heijdra YF, Nieuwenhuys R (1994): Topological analysis of the brainstem of the bowfin, Amia calva. J Comp Neurol 339:12-26.
58.
Hoogland PV, Vermeulen-Van der Zee E (1990): Distribution of choline acetyltransferase immunoreactivity in the telencephalon of the lizard Gekko gecko. Brain Behav Evol 36:378-390.
59.
Houser CR, Crawford GD, Salvaterra PM, Vaughn JE (1985): Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: a study of cholinergic neurons and synapses. J Comp Neurol 234:17-34.
60.
Huesa G, Yáñez J, Anadón R (2002): Calbindin and calretinin immunoreactivities in the retina of a chondrostean, Acipenser baeri. Cell Tissue Res 309:355-360.
61.
Hut RA, Van der Zee EA (2011): The cholinergic system, circadian rhythmicity, and time memory. Behav Brain Res 221:466-480.
62.
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.
63.
Ichikawa T, Hirata Y (1986): Organization of choline acetyltransferase-containing structures in the forebrain of the rat. J Neurosci 6:281-292.
64.
Ikeda M, Houtani T, Ueyama T, Sugimoto T (1991): Choline acetyltransferase immunoreactivity in the cat cerebellum. Neuroscience 45:671-690.
65.
Inoue JG, Miya M, Tsukamoto K, Nishida M (2003): Basal actinopterygian relationships: a mitogenomic perspective on the phylogeny of the ‘ancient fish'. Mol Phylogenet Evol 26:110-120.
66.
Jamal M, Ameno K, Miki T, Wang W, Kumihashi M, Isse T, Kawamoto T, Kitagawa K, Nakayama K, Ijiri I, Kinoshita H (2009): Cholinergic alterations following alcohol exposure in the frontal cortex of Aldh2-deficient mice models. Brain Res 1295:37-43.
67.
Jones BE, Beaudet A (1987): Distribution of acetylcholine and catecholamine neurons in the cat brainstem: a choline acetyltransferase and tyrosine hydroxylase immunohistochemical study. J Comp Neurol 261:15-32.
68.
Kanwal JS, Finger TE, Caprio J (1988): Forebrain connections of the gustatory system in ictalurid catfishes. J Comp Neurol 278:353-376.
69.
Kása P (1986): The cholinergic systems in brain and spinal cord. Prog Neurobiol 26:211-272.
70.
Kaslin J, Nystedt JM, Ostergard M, Peitsaro N, Panula P (2004): The orexin/hypocretin system in zebrafish is connected to the aminergic and cholinergic systems. J Neurosci 24:2678-2689.
71.
Kikugawa K, Katoh K, Kuraku S, Sakurai H, Ishida O, Iwabe N, Miyata T (2004): Basal jawed vertebrate phylogeny inferred from multiple nuclear DNA-coded genes. BMC Biol 2:3.
72.
Kimura H, McGeer PL, Peng JH, McGeer EG (1981): The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat. J Comp Neurol 200:151-201.
73.
King WM (1990): Nicotinic depolarization of optic nerve terminals augments synaptic transmission. Brain Res 527:150-154.
74.
King WM, Schmidt JT (1991): A cholinergic circuit intrinsic to optic tectum modulates retinotectal transmission via presynaptic nicotinic receptors. Ann NY Acad Sci 627:363-367.
75.
Lan CT, Wen CY, Tan CK, Ling EA, Shieh JY (1995): Multiple origins of cerebellar cholinergic afferents from the lower brainstem in the gerbil. J Anat 186:549-561.
76.
Lavoie B, Parent A (1994): Pedunculopontine nucleus in the squirrel monkey: distribution of cholinergic and monoaminergic neurons in the mesopontine tegmentum with evidence for the presence of glutamate in cholinergic neurons. J Comp Neurol 344:190-209.
77.
Levin ED, Simon BB (1998): Nicotinic acetylcholine involvement in cognitive function in animals. Psychopharmacology (Berl) 138:217-230.
78.
López JM, Domínguez L, Morona R, Northcutt RG, González A (2012): Organization of the cholinergic systems in the brain of two lungfishes, Protopterus dolloi and Neoceratodus forsteri. Brain Struct Funct 217:549-576.
79.
López JM, Perlado J, Morona R, Northcutt RG, González A (2013): 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.
80.
López JM, Smeets WJ, González A (2002): Choline acetyltransferase immunoreactivity in the developing brain of Xenopus laevis. J Comp Neurol 453:418-434.
81.
Lumsden A, Keynes R (1989): Segmental patterns of neuronal development in the chick hindbrain. Nature 337:424-428.
82.
Maley BE, Frick ML, Levey AI, Wainer BH, Elde RP (1988): Immunohistochemistry of choline acetyltransferase in the guinea pig brain. Neurosci Lett 84:137-142.
83.
Malz CR, Jahn H, Meyer DL (1999): Centrifugal Phe-Met-Arg-Phe-NH2-like immunoreactive innervation of the retina in a non-teleost bony fish, Lepisosteus osseus. Neurosci Lett 264:33-36.
84.
Manger PR, Fahringer HM, Pettigrew JD, Siegel JM (2002): The distribution and morphological characteristics of cholinergic cells in the brain of monotremes as revealed by ChAT immunohistochemistry. Brain Behav Evol 60:275-297.
85.
Manso MJ, Becerra M, Becerra M, Anadón R (1997): Expression of a low-molecular-weight (10 kDa) calcium binding protein in glial cells of the brain of the trout (Teleostei). Anat Embryol (Berl) 196:403-416.
86.
Marín F, Aroca P, Puelles L (2008): Hox gene colinear expression in the avian medulla oblongata is correlated with pseudorhombomeric domains. Dev Biol 323:230-247.
87.
Marín F, Puelles L (1995): Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur J Neurosci 7:1714-1738.
88.
Marín O, González A (1999): Origin of tectal cholinergic projections in amphibians: a combined study of choline acetyltransferase immunohistochemistry and retrograde transport of dextran amines. Vis Neurosci 16:271-283.
89.
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.
90.
Marín O, Smeets WJ, González A (1998): Basal ganglia organization in amphibians: chemoarchitecture. J Comp Neurol 392:285-312.
91.
Maseko BC, Manger PR (2007): Distribution and morphology of cholinergic, catecholaminergic and serotonergic neurons in the brain of Schreiber's long-fingered bat, Miniopterus schreibersii. J Chem Neuroanat 34:80-94.
92.
Mason WT, Ho YW, Eckenstein F, Hatton GI (1983): Mapping of cholinergic neurons associated with rat supraoptic nucleus: combined immunocytochemical and histochemical identification. Brain Res Bull 11:617-626.
93.
McCormick CA (1981): Central projections of the lateral line and eighth nerves in the bowfin, Amia calva. J Comp Neurol 197:1-15.
94.
McCormick CA (1982): The organization of the octavolateralis area in actinopterygian fishes: a new interpretation. J Morphol 171:159-181.
95.
Medina L, Reiner A (1994): Distribution of choline acetyltransferase immunoreactivity in the pigeon brain. J Comp Neurol 342:497-537.
96.
Medina L, Smeets WJ (1992): Cholinergic, monoaminergic and peptidergic innervation of the primary visual centers in the brain of the lizards Gekko gecko and Gallotia galloti. Brain Behav Evol 40:157-181.
97.
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.
98.
Meek J, Nieuwenhuys R (1998): Holosteans and teleosts; in Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C (eds): The Central Nervous System of Vertebrates, vol 2. Berlin, Springer, pp 759-937.
99.
Meek J, Schellart NAM (1978): A golgi study of goldfish optic tectum. J Comp Neurol 182:89-122.
100.
Mesulam MM, Geula C (1988): Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: observations based on the distribution of acetylcholinesterase and choline acetyltransferase. J Comp Neurol 275:216-240.
101.
Mesulam MM, Mufson EJ, Levey AI, Wainer BH (1984): Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience 12:669-686.
102.
Mesulam MM, Mufson EJ, Levey AI, Wainer BH (1983b): Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalmaus in the rhesus monkey. J Comp Neurol 214:170-197.
103.
Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983a): Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185-1201.
104.
Mizukawa K, McGeer PL, Tago H, Peng JH, McGeer EG, Kimura H (1986): The cholinergic system of the human hindbrain studied by choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Brain Res 379:39-55.
105.
Molist P, Maslam S, Velzing E, Roberts BL (1993): The organization of cholinergic neurons in the mesencephalon of the eel, Anguilla anguilla, as determined by choline acetyltransferase immunohistochemistry and acetylcholinesterase enzyme histochemistry. Cell Tissue Res 271:555-566.
106.
Morales-Delgado N, Merchan P, Bardet SM, Ferrán JL, Puelles L, Díaz C (2011): Topography of somatostatin gene expresion relative to molecular progenitor domains during ontogeny of the mouse hypothalamus. Front Neuroanat 5:10.
107.
Moreno N, Morona R, López JM, González A (2010): Subdivisions of the turtle Pseudemys scripta subpallium based on the expression of regulatory genes and neuronal markers. J Comp Neurol 518:4877-4902.
108.
Morita Y, Finger TE (1985): Topographic and laminar organization of the vagal gustatory system in the goldfish, Carassius auratus. J Comp Neurol 238:187-201.
109.
Morita Y, Ito H, Masai H (1980): Central gustatory paths in the crucian carp, Carassius carassius. J Comp Neurol 191:119-132.
110.
Morona R, González A (2008): Calbindin-D28k and calretinin expression in the forebrain of anuran and urodele amphibians: further support for newly identified subdivisions. J Comp Neurol 511:187-220.
111.
Morona R, González A (2009): Immunohistochemical localization of calbindin-D28k and calretinin in the brainstem of anuran and urodele amphibians. J Comp Neurol 515:503-537.
112.
Motts SD, Slusarczyk AS, Sowick CS, Schofield BR (2008): Distribution of cholinergic cells in guinea pig brainstem. Neuroscience 154:186-195.
113.
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.
114.
Mufson EJ, Cunningham MG (1988): Observations on choline acetyltransferase containing structures in the CD-1 mouse brain. Neurosci Lett 84:7-12.
115.
Mufson EJ, Desan PH, Mesulam MM, Wainer BH, Levey AI (1984): Choline acetyltransferase-like immunoreactivity in the forebrain of the red-eared pond turtle (Pseudemys scripta elegans). Brain Res 323:103-108.
116.
Mufson EJ, Martin TL, Mash DC, Wainer BH, Mesulam MM (1986): Cholinergic projections from the parabigeminal nucleus (Ch8) to the superior colliculus in the mouse: a combined analysis of horseradish peroxidase transport and choline acetyltransferase immunohistochemistry. Brain Res 370:144-148.
117.
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.
118.
Nelson JS (1994): Fish of the World, ed 3. New York, John Wiley & Sons.
119.
Nelson JS (2006): Fishes of the World, ed 4. New York, John Wiley & Sons.
120.
Nieuwenhuys R (1963): The comparative anatomy of the actinopterygian forebrain. J Hirnforsch 13:171-192.
121.
Nieuwenhuys R (1967): Comparative anatomy of the cerebellum. Prog Brain Res 25:1-93.
122.
Nieuwenhuys R (1998): Brachiopterygian Fishes; in Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C (eds): The Central Nervous System of Vertebrates, vol 2. Berlin, Springer, pp 655-699.
123.
Nieuwenhuys R (2011): The development and general morphology of the telencephalon of actinopterygian fishes: synopsis, documentation and commentary. Brain Struct Funct 215:141-157.
124.
Nieuwenhuys R, Meek J (1990): The telencephalon of actinopterygian fishes; in Jones EG, Peters A (eds): Cerebral Cortex, vol 8a. New York, Plenum Press, pp 31-73.
125.
Nieuwenhuys R, Pouwels E (1983): The brain stem of actinopterygian fishes; in Northcutt RG, Davis RE (eds): Fish Neurobiology. 1. Brain Stem and Sense Organs. Ann Arbor, University of Michigan Press, pp 25-87.
126.
Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C (1998) The Central Nervous System of Vertebrates. Berlin, Springer.
127.
Noack K, Zardoya R, Meyer A (1996): The complete mitochondrial DNA sequence of the bichir (Polypterus ornatipinnis), a basal ray-finned fish: ancient establishment of the consensus vertebrate gene order. Genetics 144:1165-1180.
128.
Northcutt RG (1982): Localization of neurons afferent to the optic tectum in longnose gars. J Comp Neurol 204:325-335.
129.
Northcutt RG (2009): Telencephalic organization in the spotted African Lungfish, Protopterus dolloi: a new cytological model. Brain Behav Evol 73:59-80.
130.
Northcutt RG, Braford MJ (1980): New observations in the organization and evolution of the telencephalon of actinopterygian fishes; in Ebesson SOE (ed): Comparative Neurology of the Telencephalon. New York, Plenum, 41-98.
131.
Northcutt RG, Butler AB (1976): Retinofugal pathways in the lingnose gar Lepisosteus osseus (linnaeus). J Comp Neurol 166:1-15.
132.
Northcutt RG, Butler AB (1980): Projections of the optic tectum in the longnose gar, Lepisosteus osseus. Brain Res 190:333-346.
133.
Northcutt RG, Butler AB (1993): The diencephalon and optic tectum of the longnose gar, Lepisosteus osseus (L.): cytoarchitectonics and distribution of acetylcholinesterase. Brain Behav Evol 41:57-81.
134.
Oh JD, Woolf NJ, Roghani A, Edwards RH, Butcher LL (1992): Cholinergic neurons in the rat central nervous system demonstrated by in situ hybridization of choline acetyltransferase mRNA. Neuroscience 47:807-822.
135.
Olsen PE (1984): The skull and pectoral girdle of the parasemionotid fish Watsonulus eugnathoides from the early triassic sakamena group of madagascar, with comments on the relationships of the holostean fishes. J Vertebr Paleontol 4:481-499.
136.
Parent A, Northcutt RG (1982): The monoamine-containing neurons in the brain of the garfish, Lepisosteus osseus. Brain Res Bull 9:189-204.
137.
Parnavelas JG, Kelly W, Franke E, Eckenstein F (1986): Cholinergic neurons and fibres in the rat visual cortex. J Neurocytol 15:329-336.
138.
Patterson C (1973): Interrelationship of holosteans; in Greenwood PH, Miles RS, Patterson C (eds): Interrelationship of Fishes. London, Academic Press, pp 233-305.
139.
Pérez SE, Yáñez 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.
140.
Perry E, Walker M, Grace J, Perry R (1999): Acetylcholine in mind: a neurotransmitter correlate of consciousness? Trends Neurosci 22:273-280.
141.
Pombal MA, El Manira A, Grillner S (1997): Organization of the lamprey striatum - transmitters and projections. Brain Res 766:249-254.
142.
Pombal MA, Marín O, González A (2001): Distribution of choline acetyltransferase-immunoreactive structures in the lamprey brain. J Comp Neurol 431:105-126.
143.
Porteros A, Gómez C, Valero J, Calvo-Baltanas F, Alonso JR (2007): Chemical organization of the macaque monkey olfactory bulb. III. Distribution of cholinergic markers. J Comp Neurol 501:854-865.
144.
Powers AS, Reiner A (1993): The distribution of cholinergic neurons in the central nervous system of turtles. Brain Behav Evol 41:326-345.
145.
Puelles E, Martínez de la Torre M, Watson C, Puelles L (2012a): Midbrain; in Watson C, Paxinos G, Puelles L (eds): The Mouse Nervous System. London, Academic Press, pp 337-359.
146.
Puelles L (1995): A segmental morphological paradigm for understanding vertebrate forebrains. Brain Behav Evol 46:319-337.
147.
Puelles L, Milán FJ, Martínez-de-la-Torre M (1996): A segmental map of architectonic subdivisions in the diencephalon of the frog Rana perezi: acetylcholinesterase-histochemical observations. Brain Behav Evol 47:279-310.
148.
Puelles L, Martínez de la Torre M, Bardet S, Rubenstein JLR. (2012b): Hypothalamus; in Watson C, Paxinos G, Puelles L (eds): The Mouse Nervous System. London, Academic Press, pp 221-312.
149.
Puelles L, Rubenstein JL (1993): Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci 16:472-479.
150.
Puelles L, Rubenstein JL (2003): Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26:469-476.
151.
Pushchina EV, Karpenko AA (2007): Distribution of cholineacetyltransferase histochemistry in isthmus and medulla of Onchorynchus masu: tract-tracing observation on the ascending meso-pontine cholinergic system (in Russian). Tsitologiia 49:581-593.
152.
Reiner A, Medina L, Veenman CL (1998): Structural and functional evolution of the basal ganglia in vertebrates. Brain Res Brain Res Rev 28:235-285.
153.
Reiner PB, Fibiger HC (1995): Psychopharmacology: the fourth generation of progress; in Bloom FE, Kupfer DJ (eds): Functional Heterogeneity of Central Cholinergic Systems. New York, Raven, pp 147-153.
154.
Rico B, Cavada C (1998): A population of cholinergic neurons is present in the macaque monkey thalamus. Eur J Neurosci 10:2346-2352.
155.
Rink E, Wullimann MF (1998): Some forebrain connections of the gustatory system in the goldfish Carassius auratus visualized by separate DiI application to the hypothalamic inferior lobe and the torus lateralis. J Comp Neurol 394:152-170.
156.
Rink E, Wullimann MF (2002): Connections of the ventral telencephalon and tyrosine hydroxylase distribution in the zebrafish brain (Danio rerio) lead to identification of an ascending dopaminergic system in a teleost. Brain Res Bull 57:385-387.
157.
Rink E, Wullimann MF (2004): Connections of the ventral telencephalon (subpallium) in the zebrafish (Danio rerio). Brain Res 1011:206-220.
158.
Roberts BL, Maslam S, Los I, Van der Jagt B (1994): Coexistence of calcitonin gene-related peptide and choline acetyltransferase in eel efferent neurons. Hear Res 74:231-237.
159.
Rodríguez-Moldes I, Molist P, Adrio F, Pombal MA, Yáñez 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.
160.
Romer AS, Persons TS (1986): The Vertebrate Body, ed 6. New York, WB Saunders Co.
161.
Rubenstein JL, Martinez S, Shimamura K, Puelles L (1994): The embryonic vertebrate forebrain: the prosomeric model. Science 266:578-580.
162.
Ruggiero DA, Giuliano R, Anwar M, Stornetta R, Reis DJ (1990): Anatomical substrates of cholinergic-autonomic regulation in the rat. J Comp Neurol 292:1-53.
163.
Rye DB, Saper CB, Lee HJ, Wainer BH (1987): Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 259:483-528.
164.
Sánchez-Camacho C, López JM, González A (2006): Basal forebrain cholinergic system of the anuran amphibian Rana perezi: evidence for a shared organization pattern with amniotes. J Comp Neurol 494:961-975.
165.
Sargent PB, Pike SH, Nadel DB, Lindstrom JM (1989): Nicotinic acetylcholine receptor-like molecules in the retina, retinotectal pathway, and optic tectum of the frog. J Neurosci 9:565-573.
166.
Satoh K, Fibiger HC (1985): Distribution of central cholinergic neurons in the baboon (Papio papio). I. General morphology. J Comp Neurol 236:197-214.
167.
Semba K (2004): Phylogenetic and ontogenetic aspects of the basal forebrain cholinergic neurons and their innervation of the cerebral cortex. Prog Brain Res 145:3-43.
168.
Smeets WJ, González A (2000): Catecholamine systems in the brain of vertebrates: new perspectives through a comparative approach. Brain Res Brain Res Rev 33:308-379.
169.
Song JK, Northcutt RG (1991): The primary projections of the lateral-line nerves of the Florida gar, Lepisosteus platyrhincus. Brain Behav Evol 37:38-63.
170.
Sorenson EM, Parkinson D, Dahl JL, Chiappinelli VA (1989): Immunohistochemical localization of choline acetyltransferase in the chicken mesencephalon. J Comp Neurol 281:641-657.
171.
Sternberger LA (1979): Immunocytochemistry. New York, John Wiley & Sons.
172.
St-Jacques R, Gorczyca W, Mohr G, Schipper HM (1996): Mapping of the basal forebrain cholinergic system of the dog: a choline acetyltransferase immunohistochemical study. J Comp Neurol 366:717-725.
173.
Straka H, Baker R, Gilland E (2006): Preservation of segmental hindbrain organization in adult frogs. J Comp Neurol 494:228-245.
174.
Striedter GF, Northcutt RG (1989): Two distinct visual pathways through the superficial pretectum in a percomorph teleost. J Comp Neurol 283:342-354.
175.
Suzuki D, Brandley MC, Tokita M (2010): The mitochondrial phylogeny of an ancient lineage of ray-finned fishes (Polypteridae) with implications for the evolution of body elongation, pelvic fin loss, and craniofacial morphology in Osteichthyes. BMC Evol Biol 10:209.
176.
Szabo T, Lazar G, Libouban S, Toth P, Ravaille M (1987): Oculomotor system of the weakly electric fish Gnathonemus petersii. J Comp Neurol 264:480-493.
177.
Tago H, McGeer PL, Bruce G, Hersh LB (1987): Distribution of choline acetyltransferase-containing neurons of the hypothalamus. Brain Res 415:49-62.
178.
Tago H, McGeer PL, McGeer EG, Akiyama H, Hersh LB (1989): Distribution of choline acetyltransferase immunopositive structures in the rat brainstem. Brain Res 495:271-297.
179.
Tumosa N, Stell WK, Johnson CD, Epstein ML (1986): Putative cholinergic interneurons in the optic tectum of goldfish. Brain Res 370:365-369.
180.
van der Zee EA, Luiten PG (1999): Muscarinic acetylcholine receptors in the hippocampus, neocortex and amygdala: a review of immunocytochemical localization in relation to learning and memory. Prog Neurobiol 58:409-471.
181.
Vanderwolf CH (1987): Near-total loss of ‘learning' and ‘memory' as a result of combined cholinergic and serotonergic blockade in the rat. Behav Brain Res 23:43-57.
182.
Varga C, Hartig W, Grosche J, Keijser J, Luiten PG, Seeger J, Brauer K, Harkany T (2003): Rabbit forebrain cholinergic system: morphological characterization of nuclei and distribution of cholinergic terminals in the cerebral cortex and hippocampus. J Comp Neurol 460:597-611.
183.
Vecino E, Ekström P (1992): Colocalization of neuropeptide Y (NPY)-like and FMRFamide-like immunoreactivities in the brain of the Atlantic salmon (Salmo salar). Cell Tissue Res 270:435-442.
184.
Venkatesh B, Erdmann MV, Brenner S (2001): Molecular synapomorphies resolve evolutionary relationships of extant jawed vertebrates. Proc Natl Acad Sci USA 98:11382-11387.
185.
Villani L, Dipietrangelo L, Pallotti C, Pettazzoni P, Zironi I, Guarnieri T (1994): Ultrastructural and immunohistochemical study of the telencephalo-habenulo-inter peduncular connections of the goldfish. Brain Res Bull 34:1-5.
186.
Vincent SR, Reiner PB (1987): The immunohistochemical localization of choline acetyltransferase in the cat brain. Brain Res Bull 18:371-415.
187.
Wainer BH, Levey AI, Mufson EJ, Mesulam MM (1984): Cholinergic systems in mammalian brain identified with antibodies against choline acetyltransferase. Neurochem Int 6:163-182.
188.
Woolf NJ (1991): Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol 37:475-524.
189.
Woolf NJ, Butcher LL (1986): Cholinergic systems in the rat brain. III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull 16:603-637.
190.
Wullimann MF (1988): The tertiary gustatory center in sunfishes is not nucleus glomerulosus. Neurosci Lett 86:6-10.
191.
Wullimann MF, Puelles L (1999): Postembryonic neural proliferation in the zebrafish forebrain and its relationship to prosomeric domains. Anat Embryol (Berl) 199:329-348.
192.
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.
193.
Yañez J, Anadón R (1996): Afferent and efferent connections of the habenula in the rainbow trout (Oncorhynchus mykiss): an indocarbocyanine dye (DiI) study. J Comp Neurol 372:529-543.
194.
Zottoli SJ, Rhodes KJ, Corrodi JG, Mufson EJ (1988): Putative cholinergic projections from the nucleus isthmi and the nucleus reticularis mesencephali to the optic tectum in the goldfish (Carassius auratus). J Comp Neurol 273:385-398.
195.
Zottoli SJ, Rhodes KJ, Mufson EJ (1987): Comparison of acetylcholinesterase and choline acetyltransferase staining patterns in the optic tectum of the goldfish Carassius auratus: a histochemical and immunocytochemical analysis. Brain Behav Evol 30:143-159.
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