Abstract
Cholinergic systems in the midbrain of the eel were identified by using histochemical procedures for the demonstration of the enzymes choline acetyltransferase (ChAT) and acetylcholinesterase. Neurons detected by both methods are located in the stratum periventriculare of the tectum, cranial motor nuclei III and IV, nucleus isthmi, nucleus gustatorius secundarius, nucleus reticularis superior, and nucleus lateralis valvulae. Some projections of these cell groups were studied by injecting horseradish peroxidase into selected brain regions. Cholinergic neurons make up about 10% of the neurons in the stratum periventriculare of the tectum and are a subset of the type-XIV neurons. Neurons in n. isthmi project primarily to the ipsilateral tectum; some cholinergic isthmal neurons project to n. pretectalis superficialis. A few ChAT-positive axons, perhaps belonging to the tectopetal system, were observed in the optic nerve. The cholinergic neurons of n. gustatorius secundarious project to the inferior lobes of the hypothalamus. The neurons of the superior reticular nucleus are a cholinergic subset of the superior reticular formation. Their axons project rostrally, probably to the thalamus and pretectum. The findings are discussed in relation to functional features of the mesencephalon, particularly in relation to locomotory control.
Similar content being viewed by others
References
Armstrong DM, Saper CB, Levey AI, Wainer BH, and Terry RD (1983) Distribution of cholinergic neurons in rat brain: demonstrated by the immunocytochemical localization of choline acetytransferase. J Comp Neurol 216:53–68
Beccari N (1943) Neurologia comparata anatomo-funzionale dei vertebrati, compreso l'uomo (Sansoni, Firenze)
Beninato M, Spencer RF (1986) A cholinergic projection to the rat supcrior colliculus demonstrated by retrograde transport of horseradish peroxidase and choline acetyltransferase immunohistochemistry. J Comp Neurol 253:525–538
Bernau NA, Puzdrowski RL, Leonard RB (1991) Identification of the midbrain locomotor region and its relation to descending locomotor pathways in the Atlantic stingray,Dasyatis sabina. Brain Res 557:83–94.
Braford MR Jr, Northcutt RG (1983) Organization of the diencephalon and pretectum of the ray-finned fishes. In: Davis RE, Northcutt RG (eds) Fish Neurobiology, vol. II, University of Michigan Press, Ann Arbor, pp 117–164
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
Brauth SE, Kitt CA, Price DL, Wainer BH (1985) Cholinergic neurons in the telencephalon of the reptileCaiman crocodilus. Neurosci Lett 58:235–240
Butchler LL (1983) Acctylcholinesterase histochemistry. In: Björklund A, Hökfelt T (eds) Handbook of Chemical Neuroanatomy, vol 1. Elsevier, Amsterdam, pp 1–49
Ciani F, Franceschini V, Del Grande P (1988) Histochemical and biochemical study on the acetylcholinesterase and choline acetyltransferase in the brain and spinal cord of frog,Rama esculenta. J Hirnforsch 2:157–163
Contestabile A, Ciani F, Villani L (1979) Ultrastructural localization of acetylcholinesterase in retino-deprived optic tectum of the goldfish. Basic and Applied. Histochemistry 23:271–277
Dammerman KW (1910) Der Saccus vasculosus der Fische, ein Tiefeorgan. Zeitschr F Wissensch Zool 96:S 654
DeLima A, Singer W (1987) The brainstem projection to the lateral geniculate nucleus in the cat: Identification of cholinergic monoaminergic elements. J Comp Neurol 259:92–121
Demski LS (1973) Feeding and aggressive behavior evoked by hypothalamic stimulation in a cichlid fish. Comp Biochem Physiol 44 A: 685–692
Deutsch JA (1983) The cholinergic synapse and the site of memory. In: Deutsch JA (ed) The physiological basis of memory, 2nd edn, Academic Press, New York, pp 351–366
Ebbesson SOE, Vanegas H (1976) Projections of the optic tectum in two teleost species. J Comp Neurol 165:161–180
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
Ekström P, Korf H-W (1986) Putative cholinergic elements in the photosensory pineal organ and retina of a teleost,Phoxinus phoxinus L. (Cyprinidae). Distribution of choline acetyltransferase immunoreactivity, acetylcholinesterase-positive elements and pinealofugally projecting neurons. Cell Tissue Res 246:321–329
Everitt BJ, Sirkiä TE, Roberts AC, Jones GH, Robbins TW (1988) Distribution and some projections of cholinergic neurons in the brain of the common marmoset,Callithrix jacchus. J Comp Neurol 271:533–558
Fite KV, Wang SR (1986) Microiontophoresis and single-unit analysis of cholinergic drugs in the optic tectum of frog. Brain Behav Evol 28:198–206
Fitzpatrick D, Conley M, Luppino G, Matelli M, Diamond IT (1988) Cholinergic projections from the midbrain reticular formation and the parabigeminal nucleus to the lateral geniculate nucleus in the tree shrew. J Comp Neurol 272:43–67
Francis A, Schechter N (1980) Regional and subcellular distribution of cholinergic enzyme and receptor activity in goldfish brain. Neuroscience 5:293–301
Grillner S, Wallen P (1984) How does the lamprey central nervous system make the lamprey swim? J Exp Biol 112:337–357
Grober MS, Bass AH, Burd G, Marchaterre MA, Segil N, Scholz K, Hodgson T (1987) The nervus terminalis ganglion inAnguilla rostrata: An immunocytochemical and HRP histochemical analysis. Brain Res 436:148–152
Groot JA, Albus H, Siegenbeek van Heukelom I (1979) A mechanistic explanation of the effect of potassium on goldfish intestinal transport. Pflügers Arch 379:1–9
Grover BG, Sharma SC (1981) Organization of extrinsic tectal connections in goldfish (Carassius auratus). J Comp Neurol 196:471–488
Gruberg ER, Udin SB (1978) Topographic projections between the nucleus isthmi and the tectum of the frogRama pipiens. J Comp Neurol 179:487–500
Ito H, Sakamoto N, Takatsuji K (1982) Cytoarchitecture, fiber connections, and ultrastructure of nucleus isthmi in a teleost (Navodon modestus) with a special reference to degenerating isthmic afferents from optic tectum and nucleus pretectalis. J Comp Neurol 205:299–311
Kashin SM, Feldman AG, Orlovsky GN (1974) Locomotion of fish evoked by electrical stimulation of the brain. Brain Res 82:41–47
King WM, Schmidt JT (1991) The long latency component of retinotectal transmission: enhancement by stimulation of nucleus isthmi or tectobulbar tract and block by nicotinic cholinergic antagonists. Neuroscience 40:701–712
Langdon RB, Freeman JA (1987) Pharmacology of retinotectal transmission in the goldfish: effects of nicotinic ligands, strychnine and kynurenic acid. J Neurosci 7:760–773
Leonard RB, Rudomin P, Droge MH, Grossman AE, Willis WD (1979) Locomotion in the decerebrate stingray. Neurosci Lett 14:315–319
Levey AI, Wainer BH (1982) Cross-species and intraspecies reactivities of monoclonal antibodies against choline acetyltransferase. Brain Res 234:469–473
Luiten PGM (1981) Afferent and efferent connections of the optic tectum in the carp (Cyprinus carpio L.). Brain Res 220:51–55
McClellan AD, Grillner S (1984) Activations of “fictive swimming” by electrical microstimulation of brainstem locomotor regions in an in vitro preparation of the lamprey central nervous system. Brain Res 300:357–361
Meek J (1990) Tectal morphology: connections, neurones and synapses. In: Douglas RH, Djamgoz MBA (eds) The visual system of fish. Chapman and Hall, London, pp 239–270
Meek J, Schellart NAM (1978) A Golgi study of goldfish optic tectum. J Comp Neurol 182:89–122
Migani P, Contestabile A, Cristini G, Labanti V (1980) Evidence of intrinsic cholinergic circuits in the optic tectum of teleosts. Brain Res 194:125–135
Milner KL, Mogenson GJ (1988) Electrical and chemical activation of the mesencephalic and subthalamic locomotor regions in freely moving rats. Brain Res 452:273–285
Mesulam MM (1982) Tracing neural connections with horseradish peroxidase. Wiley, New York
Molist P, Mos W, Maslam S, Velzing E, Roberts BL (1991) Cholinergic and locomotion-inducing systems in the midbrain of the eel. Eur J Neurosci 4 [Suppl]: 23
Morita Y, Ito H, Masai H (1980) Central gustatory paths in the crucian carp,Carassius carassius. J Comp Neurol 191:119–132
Mos W, Maslam S, Van Raamsdonk W, De Jager S (1983) Acetylcholinesterase and acetylcholine receptor histochemistry on end plate regions, myotendinous junctions and sarcolemma in the axial musculature of three teleost fish species. Acta Histochem 72:39–53
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
Nieuwenhuys R, Pouwels E (1983) The brain stem of actinopterygian fishes. In: Northcutt RG, Davis RE (eds) Fish Neurobiology vol. 1. Brain stem and sense organs. University of Michigan Press, Ann Arbor, pp 25–87
Northmore DPM (1991) Visual response of nucleus isthmi in a teleost fish (Lepomis macrochirus). Vision Res 31:525–535
Rhodes K, Zottoli S, Mufson E (1986) Choline acetyltransferase immunohistochemical staining in the goldfish (Carassius auratus) brain: evidences that the Mauthner cell does not contain choline acetyltransferase. Brain Res 381:215–224
Roberts BL, Mos W (1992) Motor programmes for speed selection in swimming fish. In: Kien J, McCrohan CR, Winlow W (eds) Neurobiology of Motor Programme Selection. Pergamon Press, Oxford, pp 123–146
Roberts BL, Meredith GE, Maslam S (1989) Immunocytochemical analysis of the dopamine system in the brain and spinal cord of the European eel,Anguilla anguilla. Anat Embryol 180:401–412
Ross CD, Godfrey DA (1986) Effect of enucleation on choline acetyltransferase activity in layers of goldfish optic tectum. Brain Res 373:49–56
Rye DB, Saper CB, Lee HJ, Wainer BH (1987) The pedunculopontine tegmental nucleus of the rat: Cytoarchitecture, cytochemistry and some extrapyramidal connectivity of the mesopontine tegmentum. J Comp Neurol 259:483–528
Sakamoto N, Ito H, Ueda S (1981) Topographic projections between the nucleus isthmi and the optic tectum in a teleostNarodon modestus. Brain Res 224:225–234
Schellart NAM, Prins M (1993) Allometry of the teleost visual system in relation to habitat and behaviour. A new approach. Neth J Zool (in press)
Schilling TF, Northeutt RG (1987) Amniotes and anamniotes may possess homoplastic retinopetal projections from the isthmic tegmentum. Soc Neurosci Abstr 13:130
Shik ML, Severin FV, Orlovsky GN (1966) Control of walking by means of electrical stimulation of the midbrain. Biophysics 11:756–765
Silver A (1974) The biology of cholinesterases. North-Holland, Amsterdam
Skinner RD, Kinjo N, Henderson V, Garcia-Rill E (1990) Locomotor projections from the pedunculopontine nucleus to spinal cord. Neuroreport 1:183–186
Takahashi Y, Okamura H, Terubayasi H, Fujisawa H, Ibata Y (1986) Retinopetal projection of LHRH-like immunoreactive neurons in the eel (Anguilla japonica) brain: combined techniques of retrograde axonal transport and immunohistochemistry in the same tissue section. Proc Int Soc Eye Res 4:62
Tumosa N, Stell WK, Johnson CD, Epstein ML (1986) Putative cholinergic interneurons in the optic tectum of goldfish. Brain Res 370:365–369
Uchiyama H (1989) Centrifugal pathways to the retina: Influence of the optic tectum. Visual Neurosci 3:183–206
Vincent SR, Reiner PB (1987) The immunohistochemical localization of choline acetyltransferase in the cat brain. Brain Res Bull 18:371–415
Wächtler K (1980) The regional production of acetylcholine in the brains of lower and higher vertebrates. Comp Biochem Physiol 65 C:1–16
Wullimann MF (1988) The tertiary gustatory center in sunfishes is not nucleus glomerulosus. Neurosci Lett 86:6–10
Zottoli SJ, Rhodes KJ, Mufson EJ (1987) Comparison of acetylcholinesterase and choline acetyltransferase staining patterns in the optic tectum of the goldfishCarassius auratus. A histochemical and immunocytochemical analysis. Brain Behav Evol 30:143–159
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
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Molist, P., Maslam, S., Velzing, E. et al. 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 (1993). https://doi.org/10.1007/BF02913740
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02913740