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The organization of afferent input to the caudal lobe of the cerebellum of the gymnotid fish Apteronotus leptorhynchus

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Summary

The caudal lobe of the cerebellum of the high frequency gymnotid fish Apteronotus leptorhynchus is that region of the cerebellum lying lateral to the posterolateral sulcus. It consists of three granular masses-the eminentia granularis posterior pars lateralis, a transitional zone T, and the eminentia granularis posterior pars medialis-with their associated molecular layers.

We have used the retrograde transport of wheat germ agglutinin conjugated horseradish peroxidase to study the afferent input to the various subdivisions of the caudal lobe. Each granular mass receives different types of input. Eminentia granularis posterior pars lateralis receives a massive bilateral input from an isthmic nucleus, nucleus praeeminentialis, concerned with descending control of the electrosensory system and from a rhombencephalic nucleus, the lateral reticular nucleus, which itself receives a major spinal input. In addition eminentia granularis posterior receives lesser input from other pretectal, (N. at base of dorsomedial optic tract, pretectal complex “B”) mesencephalic (dorsal tegmental N., nucleus raphe dorsalis), isthmic (bed N. of praeeminentialis-cerebellaris tract, locus coeruleus) and rhombencephalic nuclei (lateral tegmental N., eurydendroid cells, octaval N., perihypoglossal N., paramedian reticular N., medullary reticular formation, medullary raphe, efferent octavolateralis N., inferior olive, and funicular N.). The input from nucleus praeeminentialis dorsalis is mapped topographically onto eminentia granularis posterior with respect to their rostro-caudal location. We could not define any topography in the mapping of the dorso-ventral body axis upon eminentia granularis posterior; small injections of WGA-HRP produced several small clusters of labeled cells within nucleus praeeminentialis dorsalis which does suggest a more complex organization of this projection.

Zone T receives most of its input from the ipsilateral WIIIth nerve ganglion cells and certain pretectal nuclei, but it also receives a small input from nucleus praeeminentialis dorsalis. Eminentia granularis posterior pars medialis receives minor input from a small pretectal nucleus and a small ventral diencephalic nucleus, this region appears to receive its major input from eurydendroid cells of eminentia granularis posterior. The molecular layer associated with each granular mass receives contralateral input from separate clusters of inferior olivary cells. In addition the eurydendroid cells (cerebellar output neurons) of eminentia granularis posterior pars lateralis receive a substantial direct input from cells located in the medial aspect of nucleus praeeminentialis dorsalis.

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Abbreviations

AO :

anterior octaval nucleus

C :

cistern

CC :

corpus cerebelli

CLS :

centrolateral segment

CMS :

centromedial segment

CPTC :

caudal pretectal complex

DEC :

decussation

DML :

dorsal molecular layer

DMO Tr :

dorsomedial optic tract

D. Teg. N. :

dorsal tegmental nucleus

eff :

efferent

EGA :

eminentia granularis anterior

EGM :

eminentia granularis medialis

EGP :

eminentia granularis posterior

ELLL :

electrosensory lateral line lobe

EO :

efferent octavolateralis nucleus

ER :

electroreceptors

FN :

funicular nucleus

IO :

inferior olive

L8B :

layer 8b

LC :

lobus caudalis

LI :

interior lobe of hypothalamus

LL :

lateral lemniscuc

LLC :

lateral lemniscus commissure

LLN :

lateral line nerve

Lo. C :

locus coeruleus

LRA :

lateral reticular area

LRN :

lateral reticular nucleus

LS :

lateral segment

LTN :

lateral tegmental nucleus

ML :

molecular layer

MLF :

medial longitudinal fascieulus

MR :

medullary raphe

MS :

medial segment

NE :

nucleus electrosensorius

NG :

nucleus glomerulosus

NI :

nucleus isthmi

NLV :

nucleus lateralis valvulae

NM :

nucleus medialis

NPd :

nucleus praeeminentialis dorsalis

NPG :

nucleus preglomerulosus

NPH :

nucleus prepositus hypoglossi

NPT :

nucleus pretectalis

NRd :

nucleus raphe dorsalis

NX :

nucleus of vagus

ON :

octaval nuclei

PCA :

paratrigeminal command associated nucleus

PE-CB :

praeeminentialis cerebellaris tract

PHN :

periphypoglossal nucleus

PM :

pacemaker nucleus

PMR :

paramedian reticular nuclei

PTC “A” :

pretectal complex “A”

PTC “B” :

pretectal complex “B”

RF :

reticular formation

SP N V :

spinal nucleus of V

Te Com :

tectal commissure

Te O :

tectum opticum

Tel :

telencephalon

TL :

torus longitudinalis

TSd :

torus semicircularis dorsalis

t SF :

tractus stratum fibrosum

TSV :

torus semicircularis ventralis

V :

ventricle

VC :

valvula cerebelli

VDN :

ventral diencephalic nucleus

VML :

ventral molecular layer

WGA-HRP :

wheat germ agglutinin conjugated horeseadish peroxidase

Z “T” :

transitional zone

IV :

fourth ventricle

VIIIth N. :

elghth nerve

References

  • Barmack NH, Hess DT (1980) Eye movements evoked by microstimulation of dorsal cap of inferior olive in the rabbit. J Neurophysiol 43:163–181

    Google Scholar 

  • Bass AH (1982) Evolution of the vestibulolateral lobe of the cerebellum in electroreceptive and non-electroreceptive teleosts. J Morphol 174:335–348

    Google Scholar 

  • Bastian J (1974) Electrosensory input to the corpus cerebelli of the high frequency electric fish Eigenmannia virescens. J Comp Physiol 90:1–24

    Google Scholar 

  • Bastian J (1981) Electrolocation II: The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells in Apteronotus albifroms. J Comp Physiol 144:481–494

    Google Scholar 

  • Bastian J (1986) Gain control in the electrosensory system: a role for the descending projections to the electrosensory lateral line lobe. J Comp Physiol 158:505–515

    Google Scholar 

  • Bell CC (1984) Effects of motor commands on sensory inflow, with examples from electric fish. In: Bolis L, Keynes RD and Maddrell SHP (eds) Comparative Physiology: Sensory systems. Cambridge Univ Press, Cambridge, pp 636–647

    Google Scholar 

  • Bell CC, Libouban S, Szabo T (1983) Neural pathways related to the electric organ discharge command in mormyrid fish. J Comp Neurol 216:327–338

    Google Scholar 

  • Bell CC, Szabo T (1986) Electroreception in mormyrid fish. In: Bullock TH Heiligenberg W (eds) Electroreception. Wiley-Interscience, New York Chichester Brisbane Toronto Singapore, pp 375–421

    Google Scholar 

  • Bennett MVL, Steinbach AB (1969) Influence of electric organ control system on electrosensory afferent pathways in mormyrids. In: Llinás R (ed) Neurobiology of cerebellar evolution and development. American Association, Chicago, pp 207–214

    Google Scholar 

  • Boylls CC, Jr (1975) A theory of cerebellar function with application to locomotion. I. The physiological role of climbing fiber inputs in anterior lobe operation. In: COINS technical report. Computer and Information Science. Univ of Massachusetts, Amherst, pp 751–6

    Google Scholar 

  • Carr CC, Maler L, Heiligenberg W, Sas E (1981) Laminar organization of the afferent and efferent systems of the torus semicircularis of gymnotiform fish: Morphological substrates for parallel processing in the electrosensory system. J Comp Neurol 203:649–670

    Google Scholar 

  • Chan-Palay V, Palay SL (1971) Tendril and glomerular collaterals of climbing fibers in the granular layer of the rat's cerebellar cortex. Z Anat Entwickl Gesch 133:247–273

    Google Scholar 

  • Csillik B, Joo F, Kasa P (1963) Cholinesterase activity of archicerebellar mossy fiber apparatuses. J Histochem Cytochem 11:113–114

    Google Scholar 

  • Desclin JC, Colin F (1980) The olivocerebellar systems II. Some ultrastructural correlates of inferior olive destruction in the rat. Brain Res 187:29–46

    Google Scholar 

  • Ekström P, Van veen T (1984) Distribution of 5-hydroxytryptamine (serotonin) in the brain of the teleost gasterosteus aculeatus L. J Comp Neurol 226:307–320

    Google Scholar 

  • Finger TE (1978b) Cerebellar afferents in teleost catfish (Ictaluridae). J Comp Neurol 181:173–181

    Google Scholar 

  • Finger TE (1978b) Efferent neurons of the teleost cerebellum. Brain Res 153:608–614

    Google Scholar 

  • Finger TE (1983) The organization of the teleost cerebellum. In: Northcutt RG, Davis RE (eds) Fish Neurobiology, vol 1, Univ Michigan Press, Ann Arbor, pp 261–284

    Google Scholar 

  • Finger TE (1986) Electroreception in catfish. In: Bullock TH, Heiligenberg W (eds) Electroreception, pp 287–318

  • Finger TE, Bell CC, Carr CE (1986) Comparisons among electroreceptive teleosts: Why are electrosensory systems so similar? In: Bullock TH, Heiligenberg W (eds). Electroreception. Wiley-Interscience New York Chichester Brisbane Toronto Singapore, pp 465–482

    Google Scholar 

  • Frankenhuis-van den Heuvel THM, Niewenhuys R (1984) Distribution of serotonin-innumoreactivity in the diencephalon and mesencephalon of the trout, Salmo Gairdneri. Anat Embryol 169:193–204

    Google Scholar 

  • Hagedorn M (1986) The ecology, courtship, and mating of gymnotiform electric fish. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley Interscience, New York Chichester Brisbane Toronto, Singapore, pp 497–525

    Google Scholar 

  • Hawkes R, Colonnier M, Leclerc N (1985) Monoclonal antibodies reveal sagittal banding in the rodent cerebellar cortex. Brain Res 333:359–365

    Google Scholar 

  • Heiligenberg W (1977) Principles of electrolocation and jamming avoidance in electric fish. In: Braitenberg V (ed) Studies of brain function, vol I. Springer, Berlin, pp 1–85

    Google Scholar 

  • Ito M (1984) In: Ito M (ed) The cerebellum and neural control. Raven Press, New York

    Google Scholar 

  • Jorgensen JM (1982) Fine structure of the ampullary organs of the bichir Polypterus Senegalus (Pisces: Brachiopterygii) with some notes on the phylogenetic development of electroreceptors. Acta Zool (Stockh) 63:211–217

    Google Scholar 

  • Kah O, Chambolle P (1983) Serotonin in the brain of the goldfish, Carassius auratus. An immunocytochemical study. Cell and Tissue Res 234:319–333

    Google Scholar 

  • Kane ES, Finn RC (1977) Descending and intrinsic inputs to dorsal cochlear nucleus of cats: A horseradish peroxidase study. Neurosci 2:897–912

    Google Scholar 

  • Kotchabhakdi N, Walberg F (1978) Primary vestibular afferent projections to the cerebellum as demonstrated by retrograde axonal transport of horseradish peroxidase. Brain Res 142:142–146

    Google Scholar 

  • Libouban M, Szabo T (1977) An integration centre of the mormyrid fish brain: The auricula cerebelli. An HRP study. Neurosci Lett 6:115–119

    Google Scholar 

  • Llinás R (1982) General discussion: Radial connectivity in the cerebellar cortex: A novel view regarding the functional organization of the molecular layer. In: Palay SL, Chan-Palay V (eds) The cerebellum. New vistas. Springer, Berlin Heidelberg New York, pp 189–194

    Google Scholar 

  • Maekawa K, Kimura M (1981) Electrophysiological study of the nucleus of the optic tract that transfers optic signals to the nucleus reticularis tegmenti pontis—the visual mossy fibre pathway to the cerebellar floculus. Brain Res 211:456–462

    Google Scholar 

  • Maekawa K, Takeda T (1977) Afferent pathways from the visual system to the cerebellar flocculus of the rabbit. In: Baker R, Berthos A (eds) Control of gaze by brain stem neurons. Elsevier, Amsterdam, pp 187–195

    Google Scholar 

  • Maler L (1979) The posterior lateral line lobe of certain gymnotid fish. Quantitative light microscopy. J Comp Neurol 183:323–363

    Google Scholar 

  • Maler L, Finger T, Karten H (1974) Differential projections of ordinary lateral line and electroreceptors in the gymnotid fish, Apteronotus albifrons. J Comp Neurol 158:363–382

    Google Scholar 

  • Maler L, Collins M, Mathieson NB (1981) The distribution of acetylcholinesterase and choline acetyl transferase in the cerebellum and posterior lateral line lobe of weakly electric fish (gymnotidae). Brain Res 226:320–325

    Google Scholar 

  • Maler L, Sas E, Carr CE, Matsubara J (1982) Efferent projections of the posterior lateral line lobe in gymnotiform fish. J Comp Neurol 211:154–164

    Google Scholar 

  • Maler L, Jande S, Lawson EM (1984) Localization of vitamin D-dependant calcium binding protein in the electrosensory and electromotor systems of high frequency gymnotid fish. Brain Res 301:166–170

    Google Scholar 

  • Matsubara J, Finger TE, Maler L, Carr CE (1981) Electrosensory, auditory and lateral line nuclei in the midbrain of a gymnotiform weakly electric fish, Sternopygus. Soc Neurosci Abstr 7:84

    Google Scholar 

  • McCormick CA (1981) Central projections of the lateral line and eight nerves in the bowfin, Amia calva. J Comp Neurol 197:1–15

    Google Scholar 

  • McCormick CA (1983) Organization and evolution of the octavolateralis area of fishes. In: Northcutt RG, Davis RE (eds) Fish Neurobiology, vol I. Univ of Michigan Press, Ann Arbor, pp 179–213

    Google Scholar 

  • Mesulam MM (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106–117

    Google Scholar 

  • Mugnaini, E (1972) The histology and cytology of the cerebellar cortex. In: Larsell O, Jansen J (eds) The comparative anatomy and histology of the cerebellum: The human cerebellum cerebellar connections and cerebellar cortex Univ of Minnesota Press, Minneapolis, pp 201–265

    Google Scholar 

  • Mugnaini E, Warr WB, Osen KK (1980a) Distribution and light microscopic features of granule cells in the cochlear nuclei of cat, rat and mouse. J Comp Neurol 195:581–606

    Google Scholar 

  • Mugnaini E, Osen KK, Dahl AL, Fredrick VL, Korte G (1980b) Fine structure of granule cells and related interneurons (termed Golgi cells) in the cochlear nuclear complex of cat, rat and mouse. J Neurocytol 9:537–570

    Google Scholar 

  • Mugnaini E (1985) GABA neurons in the superficial layers of the rat dorsal cochlear nucleus: light and electron microscopic immunocytochemistry. J Comp Neurol 235:61–81

    Google Scholar 

  • Nelson B, Mugnaini E (1985) Loss of gabaergic nerve terminals in the inferior olive and cerebellectomized rats. Soc Neurosci Abstr 11:182

    Google Scholar 

  • Nieuwenhuys R, Nicholson (1969) Aspects of the histology of the cerebellum of mormyrid fishes. In: Llinás R (ed) Neurobiology of cerebellar evolution and development. Am Med Assn Educ Res Fdn, pp 135–169

  • Osen KK, Mugnaini E, Dahl AL, Christiansen AH (1984) Histochemical localization of acetylcholinesterase in the cochlear and superior olivary nuclei. A reappraisal with emphasis on the cochlear granule cell system. Arch Ital Biol 122:164–212

    Google Scholar 

  • Palay SL, Chan-Palay V (1974) Cerebellar cortex: Cytology and organization. Springer, New York, pp 1–348

    Google Scholar 

  • Parent A (1983) The monoamine-containing neuronal systems in the teleostean brain. In: Davis RE Northcutt RG (eds) Fish neurobiology, vol 2. The University of Michigan Press, Ann Arbor, pp 285–315

    Google Scholar 

  • Parent A, Dube, L, Braford MR, Northcutt RG (1978) The organisation of monoamine-containing neurons in the brain of the sunfish (lepomis gibbosus) as revealed by fluorescence microscopy. J Comp Neurol 182:495–516

    Google Scholar 

  • Pellionisz A, Llinás R (1982) The tensor concept of brain function: A theory of the cerebellum. In: Amari S, Arbib MA (eds) Competition and cooperation in neural nets. Springer, Berlin Heidelberg new York, pp 394–417

    Google Scholar 

  • Pierce ET (1967) Histogenesis of the dorsal and ventral cochlear nuclei in the mouse. An autoradiographic study. J Comp Neurol 131:27–54

    Google Scholar 

  • Precht W (1978) In: Braintenberg V (ed) Neuronal operations in the vestibular system, vol 2. Springer, Berlin Heidelberg New York, pp 154–160

    Google Scholar 

  • Precht W, Simpson J, Llinás R (1976) Responses of Purkinje cells in rabbit nodulus and uvula to natural vestibular and visual stimuli. Pflügers Arch 367:1–16

    Google Scholar 

  • Roberts BL (1984) Role of sensory information in the control of locomotion in fishes. In: Bolis L, Keynes RD, Maddrell SHP (eds) Comparative physiology of sensory systems. Cambridge University Press. Cambridge, London New York New Rochelle Melbourne Sydney, pp 623–636

    Google Scholar 

  • Sas E, Maler L (1983) The nucleus praeeminentialis: A Golgi study of a feedback center in the electrosensory system of gymnotid fish. J Comp Neurol 221:127–144

    Google Scholar 

  • Sas E, Maler L (1985) The connectivity of a cerebellar structure (eminentia granularis pars posterior) in the teleost Apteronotus leptorhynchus. Soc Neurosci Abstr 11:693

    Google Scholar 

  • Sas E, Maler L (1986) Retinofugal projections in a weakly electric gymnotid fish (Apteronotus leptorhynchus). Neurosci 18:247–259

    Google Scholar 

  • Shumway CA (1986) Physiological differences in the multiple maps of the electrosensory lateral line lobe: pyramidal cells have different receptive field sizes. Soc Neurosci Abstr 12:201

    Google Scholar 

  • Szabo T, Libouban S, Haugedé-Carré F (1979) Convergence of common and specific sensory afferents to the crebellar auricle (auricle cerebelli) in the teleost fish gnathonemus demonstrated by HRP method. Brain Res 168:619–622

    Google Scholar 

  • Tolbert DL, Bantli H, Bloedel JR (1978) Organizational features of the cat and monkey cerebellar nucleocortical projection. J Comp Neurol 182:39–56

    Google Scholar 

  • Tong SL, Bullock TH (1982) Electroreceptive representation and its dynamics in the cerebellum of the catfish, Ictalurus nebulosus. J Comp Physiol 145:289–298

    Google Scholar 

  • Tong SL, Finger TE (1983) Central organization of the electrosensory lateral line system in bullhead catfish, Ictalurus nebulosus. J Comp neurol 217:1–16

    Google Scholar 

  • Yingcharoen K, Rinvik E (1982) Branched projections from the nucleus prepositus hypoglossi to the oculomotor nucleus and the cerebellum. A retrograde fluorescent double-labeling study in the Cat. Brain Res 246:133–136

    Google Scholar 

  • Zakon H (1986) The electroreceptive periphery. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley-Interscience, New York Chichester Brisbane Toronto Singapore, pp 103–156

    Google Scholar 

Download references

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Authors and Affiliations

  1. Department of Anatomy, Faculty of Health Sciences, School of Medicine, University of Ottawa, Ottawa, Ontario, Canada

    Emilia Sas & Leonard Maler

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  1. Emilia Sas
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  2. Leonard Maler
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Sas, E., Maler, L. The organization of afferent input to the caudal lobe of the cerebellum of the gymnotid fish Apteronotus leptorhynchus . Anat Embryol 177, 55–79 (1987). https://doi.org/10.1007/BF00325290

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