Distribution of choline acetyltransferase (ChAT) immunoreactivity in the central nervous system of a chondrostean, the siberian sturgeon (Acipenser baeri)

All studies to date of cholinergic systems of bony fishes have been done in teleosts. To gain further insight into the evolution of the cholinergic systems of bony fishes, we have studied the brain of a chondrostean fish, the Siberian sturgeon (Acipenser baeri, Brandt), by using an antibody against choline acetyltransferase (ChAT). This study showed the presence of ChAT‐immunoreactive (ChAT‐ir) neurons in the preoptic region (parvocellular and magnocellular preoptic nuclei and suprachiasmatic nucleus), the periventricular and tuberal hypothalamus, the saccus vasculosus, the dorsal thalamus, and the habenula. The mesencephalic tegmentum contained ChAT‐ir cells in the torus semicircularis and torus lateralis. The isthmus contained several cholinergic populations: the nucleus isthmi, the lateral nucleus of the valvula, the secondary visceral nucleus, and the dorsal tegmental nucleus. The motor neurons of the cranial nerves and the spinal motor column were strongly immunoreactive. The medial (sensory) trigeminal nucleus also contained a ChAT‐ir neuronal population. The distribution of ChAT‐ir neurons in the sturgeon brain showed some notable differences with that observed in teleosts, such as the absence of cholinergic cells in the telencephalon and the optic tectum. Several brain regions were richly innervated by ChAT‐ir fibers, particularly the telencephalon , optic tectum, thalamus, posterior tubercle, and interpeduncular nucleus. The hypothalamo‐hypophyseal tract, the tract of the saccus vasculosus, the fasciculus retroflexus, and an isthmo‐mesencephalo‐thalamic tract were the most conspicuous cholinergic bundles. Comparative analysis of these results suggests that teleosts have conserved most traits of the cholinergic system of the sturgeon, having acquired new cholinergic populations during evolution. J. Comp. Neurol. 426:602–621, 2000. © 2000 Wiley‐Liss, Inc.

[1]  W. Chavin,et al.  Hypothalamo-hypophyseal neurosecretory system in the primitive actinopterygian fishes (Holostei and Chondrostei). , 1967, Acta anatomica.

[2]  L. Sternberger,et al.  THE UNLABELED ANTIBODY ENZYME METHOD OF IMMUNOHISTOCHEMISTRY PREPARATION AND PROPERTIES OF SOLUBLE ANTIGEN-ANTIBODY COMPLEX (HORSERADISH PEROXIDASE-ANTIHORSERADISH PEROXIDASE) AND ITS USE IN IDENTIFICATION OF SPIROCHETES , 1970, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[3]  W. Jansen,et al.  A cytochemical investigation of specific and non-specific cholinesterase activity in the saccus vasculosus of the rainbow trout. , 1971, Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen. Series C. Biological and medical sciences.

[4]  M. Dubois,et al.  [Immunofluorescence demonstration of glycoproteic hormone producing cells in the hypophysis of an Iranian rodent, (Ellobius lutescens (Th): gonadotropic and thyrotropic cells]. , 1972, Zeitschrift fur Zellforschung und mikroskopische Anatomie.

[5]  T. J. Voneida,et al.  A comparative neuroanatomic study of retinal projections in two fishes: Astyanax hubbsi (the blind cave fish), and Astyanax mexicanus , 1976, The Journal of comparative neurology.

[6]  G. Wolf.  Immunohistological identification of neurophysin and neurophysin-like substances in different vertebrates. , 1976, Endokrinologie.

[7]  M. Jones,et al.  The effect of dopamine on neurohypophysial hormone release in vivo and from the rat neural lobe and hypothalamus in vitro. , 1976, The Journal of physiology.

[8]  T. Finger.  Gustatory pathways in the bullhead catfish. II. Facial lobe connections , 1978, The Journal of comparative neurology.

[9]  A. Hodgson,et al.  Acetylcholinesterase hydrolyzes substance P , 1980, Neuroscience.

[10]  Hironobu Ito,et al.  Central gustatory paths in the crucian carp, carassius carassius , 1980, The Journal of comparative neurology.

[11]  H. Thoenen,et al.  Production of specific antibodies to choline acetyltransferase purified from pig brain , 1981, Neuroscience.

[12]  N. Sakamoto,et al.  Topographic projections between the nucleus isthmi and the optic tectum in a teleost,Navodon Modestus , 1981, Brain Research.

[13]  P. Luiten.  Afferent and efferent connections of the optic tectum in the carp (Cyprinus carpio L.) , 1981, Brain Research.

[14]  J. Stein,et al.  Depression of nigral pars compacta cell discharge by exogenous acetylcholinesterase , 1981, Neuroscience.

[15]  N. Vesselkin,et al.  The retinofugal pathways in a primitive actinopterygian, the chondrostean Acipenser güldenstädti. An experimental study using degeneration, radioautographic and HRP methods , 1982, Brain Research.

[16]  F. Eckenstein,et al.  Mapping of cholinergic neurons associated with rat supraoptic nucleus: Combined immunocytochemical and histochemical identification , 1983, Brain Research Bulletin.

[17]  A. Levey,et al.  Distribution of cholinergic neurons in rat brain: Demonstrated by the immunocytochemical localization of choline acetyltransferase , 1983, The Journal of comparative neurology.

[18]  H. Vanegas,et al.  Morphological aspects of the teleostean visual system: A review , 1983, Brain Research Reviews.

[19]  J. E. Vaughn,et al.  Organization and morphological characteristics of cholonergic neurons: an immunocytochemical study with a monoclonal antibody to choline acetyltransferase , 1983, Brain Research.

[20]  H. Thoenen,et al.  Cholinergic neurons in the rat cerebral cortex demonstrated by immunohistochemical localization of choline acetyltransferase , 1983, Neuroscience Letters.

[21]  R. Northcutt,et al.  Central projections of the lateral line nerves in the shovelnose sturgeon , 1984, The Journal of comparative neurology.

[22]  M. Mesulam,et al.  Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry , 1984, Neuroscience.

[23]  M. Mesulam,et al.  Choline acetyltransferase-immunoreactive neurons intrinsic to rodent cortex and distinction from acetylcholinesterase-positive neurons , 1984, Neuroscience.

[24]  M. Mesulam,et al.  Choline acetyltransferase-like immunoreactivity in the forebrain of the red-eared pond turtle (Pseudemys scripta elegans) , 1984, Brain Research.

[25]  Cholinergic systems in mammalian brain identified with antibodies against choline acetyltransferase , 1984, Neurochemistry International.

[26]  R. Northcutt,et al.  Primary projections of the trigeminal nerve in two species of sturgeon: Acipenser oxyrhynchus and Scaphirhynchus platorynchus , 1984, Journal of morphology.

[27]  V. V. Kuzik,et al.  The Hypothalamo-Hypophyseal System in Acipenseridae☆ , 1985 .

[28]  C. Gregg.  The compartmentalized hypothalamo-neurohypophysial system: evidence for a neurohypophysial action of acetylcholine on vasopressin release. , 1985, Neuroendocrinology.

[29]  K. Kotrschal,et al.  Distribution of aminergic neurons in the brain of the sterlet, Acipenser ruthenus (Chondrostei, Actinopterygii). , 1985, Journal fur Hirnforschung.

[30]  E. Gruberg,et al.  Nucleus isthmi provides most tectal choline acetyltransferase in the frogRana pipiens , 1985, Brain Research.

[31]  H. Fibiger,et al.  Distribution of central cholinergic neurons in the baboon (papio papio). I. General morphology , 1985, The Journal of comparative neurology.

[32]  D. Price,et al.  Cholinergic neurons in the telencephalon of the reptile Caiman crocodilus , 1985, Neuroscience Letters.

[33]  B. L. Roberts,et al.  Central organization of the efferent supply to the labyrinthine and lateral line receptors of the dogfish , 1986, Neuroscience.

[34]  R. Baker,et al.  Organization of the efferent, vestibular nuclei and nerves of the toadfish, Opsanus tau , 1986, The Journal of comparative neurology.

[35]  F. Eckenstein,et al.  Cholinergic neurons and fibres in the rat visual cortex , 1986, Journal of neurocytology.

[36]  W. Stell,et al.  Putative cholinergic interneurons in the optic tectum of goldfish , 1986, Brain Research.

[37]  R. Spencer,et al.  A cholinergic projection to the rat superior colliculus demonstrated by retrograde transport of horseradish peroxidase and choline acetyltransferase immunohistochemistry , 1986, The Journal of comparative neurology.

[38]  D. Mash,et al.  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 , 1986, Brain Research.

[39]  L. Maler,et al.  Identification of a nucleus isthmi in the weakly electric fish Apteronotus leptorhynchus (Gymnotiformes). , 1986, Brain, behavior and evolution.

[40]  J. E. Vaughn,et al.  Immunocytochemical localization of choline acetyltransferase in rat ventral striatum: a light and electron microscopic study , 1986, Journal of neurocytology.

[41]  M. Geffard,et al.  The dopaminergic innervation of the goldfish pituitary. An immunocytochemical study at the electron-microscope level using antibodies against dopamine. , 1986, Cell and tissue research.

[42]  L. Hersh,et al.  Distribution of choline acetyltransferase-containing neurons of the hypothalamus , 1987, Brain Research.

[43]  B. L. Roberts,et al.  Immunohistochemical study of a dopaminergic system in the spinal cord of the ray, Raja radiata , 1987, Brain Research.

[44]  P. Ekström.  Distribution of choline acetyltransferase‐immunoreactive neurons in the brain of a cyprinid teleost (Phoxinus phoxinus L.) , 1987, The Journal of comparative neurology.

[45]  K. Rhodes,et al.  Comparison of acetylcholinesterase and choline acetyltransferase staining patterns in the optic tectum of the goldfish Carassius auratus. A histochemical and immunocytochemical analysis. , 1987, Brain, behavior and evolution.

[46]  H. Killackey,et al.  Choline acetyltransferase-immunoreactive neurons in fetal monkey cerebral cortex. , 1987, Brain research.

[47]  P. Groves,et al.  Relation of pontine choline acetyltransferase immunoreactive neurons with cells which increase discharge during REM sleep , 1987, Brain Research Bulletin.

[48]  P. Reiner,et al.  The immunohistochemical localization of choline acetyltransferase in the cat brain , 1987, Brain Research Bulletin.

[49]  F. Eckenstein,et al.  Cholinergic innervation of the optic tectum in the frogRana pipiens , 1987, Brain Research.

[50]  T. Finger,et al.  Forebrain connections of the gustatory system in ictalurid catfishes , 1988, The Journal of comparative neurology.

[51]  A. Levey,et al.  Immunohistochemistry of choline acetyltransferase in the guinea pig brain , 1988, Neuroscience Letters.

[52]  F. Gage,et al.  Cholinergic neurons within the rat hippocampus: Response to fimbria‐fornix transection , 1988, The Journal of comparative neurology.

[53]  E. Mufson,et al.  Putative cholinergic projections from the nucleus isthmi and the nucleus reticularis mesencephali to the optic tectum in the goldfish (Carassius auratus) , 1988, The Journal of comparative neurology.

[54]  E. Mufson,et al.  Observations on choline acetyltransferase containing structures in the CD-1 mouse brain , 1988, Neuroscience Letters.

[55]  T. Robbins,et al.  Distribution and some projections of cholinergic neurons in the brain of the common marmoset, Callithrix jacchus , 1988, The Journal of comparative neurology.

[56]  M. Wullimann.  The tertiary gustatory center in sunfishes is not nucleus glomerulosus , 1988, Neuroscience Letters.

[57]  K. Rhodes,et al.  Localization of choline acetyltransferase to somata of posterior lateral line efferents in the goldfish , 1988, Brain Research.

[58]  A. Bass,et al.  Cholinergic neurons in the brain of a teleost fish (Porichthys notatus) located with a monoclonal antibody to choline acetyltransferase , 1988, The Journal of comparative neurology.

[59]  L. Hersh,et al.  Distribution of choline acetyltransferase immunopositive structures in the rat brainstem , 1989, Brain Research.

[60]  V. Chiappinelli,et al.  Immunohistochemical localization of choline acetyltransferase in the chicken mesencephalon , 1989, The Journal of comparative neurology.

[61]  K. Fuxe,et al.  Evidence for the existence of a population of arcuate neurons costoring choline acetyltransferase and tyrosine hydroxylase immunoreactivities in the male rat , 1989, Neuroscience Letters.

[62]  P. Hoogland,et al.  Distribution of choline acetyltransferase immunoreactivity in the telencephalon of the lizard Gekko gecko. , 1990, Brain, behavior and evolution.

[63]  M. Wullimann,et al.  Visual and electrosensory circuits of the diencephalon in mormyrids: An evolutionary perspective , 1990, The Journal of comparative neurology.

[64]  Nancy J. Woolf,et al.  Cholinergic systems in mammalian brain and spinal cord , 1991, Progress in Neurobiology.

[65]  A. Reiner,et al.  A comparison of neurotransmitter-specific and neuropeptide-specific neuronal cell types present in the dorsal cortex in turtles with those present in the isocortex in mammals: implications for the evolution of isocortex. , 1991, Brain, behavior and evolution.

[66]  B. Borg,et al.  Development of tyrosine hydroxylase-, dopamine- and dopamine β-hydroxylase-immunoreactive neurons in a teleost, the three-spined stickleback , 1992, Journal of Chemical Neuroanatomy.

[67]  N. Schellart,et al.  The pattern of trunk lateral line afferents and efferents in the rainbow trout (Salmo gairdneri). , 1992, Brain, behavior and evolution.

[68]  G. Roth,et al.  Is the nucleus corticalis of teleosts a new cholinergic central nervous system for vertebrates? , 1992, Neuroreport.

[69]  H. Steinbusch,et al.  Distribution of dopamine immunoreactivity in the brain of the mormyrid teleost Gnathonemus petersii , 1989, The Journal of comparative neurology.

[70]  J. Schmidt,et al.  Nucleus isthmi in goldfish: In vitro recordings and fiber connections revealed by HRP injections , 1993, Visual Neuroscience.

[71]  A. Reiner,et al.  The distribution of cholinergic neurons in the central nervous system of turtles. , 1993, Brain, behavior and evolution.

[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]  I. Zironi,et al.  Choline acetyltransferase and NADPH-diaphorase localization in the goldfish habenulo-interpeduncular system , 1994, Neuroscience Letters.

[74]  A. Chiba,et al.  Neuropeptide Y-immunoreactive structures in the telencephalon and diencephalon of the white sturgeon, Acipenser transmontanus, with special regard to the hypothalamo-hypophyseal system. , 1994, Archives of histology and cytology.

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

[76]  Ivan P. Los,et al.  Coexistence of calcitonin gene-related peptide and choline acetyltransferase in EEL efferent neurons , 1994, Hearing Research.

[77]  B. L. Roberts,et al.  Dopaminergic and GABAergic cerebrospinal fluid‐contacting neurons along the central canal of the spinal cord of the eel and trout , 1995, The Journal of comparative neurology.

[78]  W. L. Strauss,et al.  The Human Choline Acetyltransferase Gene Encodes Two Proteins , 1995, Journal of neurochemistry.

[79]  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.

[80]  W. Gorczyca,et al.  Mapping of the basal forebrain cholinergic system of the dog: A choline acetyltransferase immunohistochemical study , 1996, The Journal of comparative neurology.

[81]  M. Schäfer,et al.  Visualization of the vesicular acetylcholine transporter in cholinergic nerve terminals and its targeting to a specific population of small synaptic vesicles. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[82]  R. Anadón,et al.  The neuronal system of the saccus vasculosus of trout (Salmo trutta fario and Oncorhynchus mykiss): an immunocytochemical and nerve tracing study , 1997, Cell and Tissue Research.

[83]  R. Ward,et al.  Immunocytochemical localization of dopamine and its synthetic enzymes in the central nervous system of the lamprey Lampetra fluviatilis , 1997, The Journal of comparative neurology.

[84]  K. Ajiki,et al.  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 , 1997, Journal of Chemical Neuroanatomy.

[85]  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.

[86]  S. Álvarez.  Estudio de la distribución en el SNC de marcadores de sistemas colinérgicos durante el desarrollo y etapa adulta de la trucha mediante técnicas histoquímicas e inmunohistoquímicas , 1998 .

[87]  B. Rupp,et al.  The Diencephalon and Pretectum of the White Sturgeon (Acipenser transmontanus): A Cytoarchitectonic Study , 1998, Brain, Behavior and Evolution.

[88]  R. Anadón,et al.  Neural connections of the pineal organ in the primitive bony fish Acipenser baeri: A carbocyanine dye tract‐tracing study , 1998, The Journal of comparative neurology.

[89]  J. Albert,et al.  Tectal Fiber Connections in a Non-Teleost Actinopterygian Fish, the Sturgeon Acipenser , 1999, Brain, Behavior and Evolution.

[90]  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.

[91]  J. Albert,et al.  Retinal Projections and Retinal Ganglion Cell Distribution Patterns in a Sturgeon (Acipenser transmontanus), a Non-Teleost Actinopterygian Fish , 1999, Brain, Behavior and Evolution.

[92]  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.

[93]  O. Marín,et al.  Origin of tectal cholinergic projections in amphibians: A combined study of choline acetyltransferase immunohistochemistry and retrograde transport of dextran amines , 1999, Visual Neuroscience.

[94]  O. Marín,et al.  Choline acetyltransferase immunoreactivity in the hypothalamoneurohypophysial system of the lamprey. , 1999, European journal of morphology.

[95]  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.

[96]  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.