Skip to main content
Log in

A simple cerebellar system: The lateral line lobe of the goldfish

  • Published:
Journal of comparative physiology Aims and scope Submit manuscript

Summary

  1. 1.

    The lateral line lobe consists of two structures, a layer of cerebellar material, the crista cerebelli overlying the medullary gray. Field potentials and single cell recordings made after stimulating the lateral line nerve and the caudal lobe of the cerebellum show that the primitive Purkinje cells (pP cells) of the crista can be excited by stimulating the large parallel fibre input running from the caudal lobe and (some cells) by stimulating the lateral line nerve. The parallel fibres do not appear to be involved in these latter responses and their role is unknown.

  2. 2.

    Apart from the extrinsic origin of the parallel fibres the crista cerebelli also differs from the cerebellum by having no identifiable climbing fibres. Stellate cell inhibition however appears to be present.

  3. 3.

    The small secondary lateral line cells in the gray layer receive punctate primary afferent inputs from one lateral line organ and a diffuse polysynaptic inhibitory input which can be seen as ipsps evoked in anterior lateral line gray cells by posterior lateral line nerve stimulation.

  4. 4.

    The lateral line inputs to the pP cells are highly variable and, in contrast to the gray cells pP cells show diffuse receptive fields when tested with “natural” stimuli.

  5. 5.

    Stimulation of the pP cells inhibits the gray cells and it seems that they are responsible for the inhibitory effect noted in (3).

  6. 6.

    It is suggested that pP cells with diffuse receptive fields inhibiting gray cells with punctate receptive fields could form a sensory lateral inhibition mechanism in the lateral line lobe.

  7. 7.

    When the responses of primary fibres in the lateral line nerve and secondary lateral line gray cells to measured physiological stimuli (water displacements at 30 Hz) are compared such a lateral inhibition seems to be present in the lateral line lobe. Secondary gray cells have response attenuation curves of 6–17 dB/cm as the stimulating probe is moved away from the units receptive field. The primary fibres show symmetrical curves with slopes of 4–6 dB/cm which corresponds to the calculated stimulus attenuation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

alln:

anterior lateral line nerves

co:

commissure

crista:

crista cerebelli

ext gran:

external granule cell layer of the caudal lobe of the corpus cerebelli

gran:

granule cell layer of the corpus cerebelli

gray:

medullary gray of Pearson

mc:

Mauthner cell

mlf:

medial longitudinal fasciculus

mol:

molecular layer of corpus cerebelli

pl:

plexus of axons at the dorsal limit of the gray

plln:

posterior lateral line nerve

pP cells:

primitive Purkinje cells

2 gust:

ascending secondary gustatory tract

IV:

fourth ventricle

VII:

descending root of nerve VII

VIII:

nerve VIII

References

  • Alnaes, E.: Two types of lateral line afferents in the eel (Anguilla anguilla). Acta Physiol. Scand.87, 535–548 (1973a)

    Google Scholar 

  • Alnaes, E.: Lateral line input to the crista cerebellaris in the eel. Field potentials and histology. Acta Physiol. Scand.88, 49–61 (1973b)

    Google Scholar 

  • Alnaes, E.: Unit activity of ganglionic and medullary second order neurons in the eel lateral line system. Acta Physiol. Scand.88, 160–174 (1973c)

    Google Scholar 

  • Altman, J.: Experimental reorganisation of cerebellar cortex in the rat. IV. Parallel fibre reorientation following regeneration of the external germinal layer. J. comp. Neurol.149, 181–191 (1973)

    Google Scholar 

  • Andrianov, G.N., Ilyinsky, O.B.: Some functional properties of central neurons connected with the lateral line organs of the catfish,Ictalurus nebulosus. J. comp. Physiol.86, 365–376 (1973)

    Google Scholar 

  • Ariens Kappers, C.U., Huber, C.G., Crosby, E.C.: The comparative anatomy of the central nervous system of vertebrates including man, Vol. 1. New York: Hafner 1967; 1st Pub. Macmillan 1936

    Google Scholar 

  • Banner, A.: Propagation of sound in a shallow bay. J. Acoust. Soc. Am.49, 373–376 (1971)

    Google Scholar 

  • Berry, M., Bradley, P.M.: The application of network analysis to the study of branching patterns of large dendritic fields. Brain Res.109, 111–132 (1976a)

    Google Scholar 

  • Berry, M., Bradley, P.M.: The growth of the dendritic trees of Purkinje cells in the cerebellum of the rat. Brain Res.112, 1–35 (1976b)

    Google Scholar 

  • Britt, R., Starr, A.: Synaptic events and discharge patterns of cochlear nucleus cells. 1. Steady frequency tone bursts. J. Neurophysiol.39, 162–178 (1976a)

    Google Scholar 

  • Britt, R., Starr, A.: Synaptic events and discharge patterns of cochlear nucleus cells. 2. Frequency modulated tones. J. Neurophysiol.39, 179–194 (1976b)

    Google Scholar 

  • Djikgraaf, S.: The function and significance of the lateral line organs. Biol. Rev.38, 51–105 (1963)

    Google Scholar 

  • Eccles, J.C., Ito, M., Szentagothai, J.: The cerebellum as a neuronal machine. Berlin-Heidelberg-New York: Springer 1967

    Google Scholar 

  • Eccles, J.C., Taborikora, H., Tsukahara, N.: Responses of the Purkinje cells of a selachian cerebellum (Mustelus canis). Brain Res.17, 57–86 (1970)

    Google Scholar 

  • Evans, E.F., Palmer, A.R.: Responses of units in the cochlear nerve and nucleus of the cat to signals in the presence of bandstop noise. J. Physiol.252, 60–62 p (1975)

    Google Scholar 

  • Faber, D.S., Korn, H.: Inhibition in frog cerebellar cortex following parallel fibre activation. Brain Res.17, 506–510 (1970)

    Google Scholar 

  • Flock, Å.: The lateral line organ mechanoreceptors. In: Fish physiology, Vol. 5 (eds. W.S. Hoar, D.J. Randall), pp. 241–264. New York-London: Academic Press 1971

    Google Scholar 

  • Flock, Å., Jorgensen, M., Russell, I.J.: The physiology of individual hair cells and their synapses. In: Basic mechanisms in hearing (ed. A.R. Møller). New York-London: Academic Press 1973

    Google Scholar 

  • Flock, Å., Russell, I.J.: Efferent nerve fibres, postsynaptic action of hair cells. Nature243, 89–91 (1973a)

    Google Scholar 

  • Flock, Å., Russell, I.J.: The postsynaptic action of efferent fibres in the lateral line organ of the Barbot,Lota lota. J. Physiol.235, 591–605 (1973b)

    Google Scholar 

  • Freeman, J.A.: The cerebellum as a timing device, an experimental study in the frog. In: Neurobiology of cerebellar evolution and development (ed. R. Llinás). Chicago: Amer. Med. Ass. 1969

    Google Scholar 

  • Freeman, J.A., Nicholson, C.: Experimental optimisation of current source density technique for anuran cerebellum. J. Neurophysiol.38, 369–382 (1975)

    Google Scholar 

  • Fukuda, J.: Fibre composition of the posterior lateral line nerve investigated by electrophysiological and microscopical techniques. J. comp. Neurol.155, 203–218 (1974)

    Google Scholar 

  • Fuller, P.M., Prior, D.J.: Cobalt iontophoresis techniques for tracing afferent and efferent connections in vertebrate CNS. Brain Res.88, 211–220 (1975)

    Google Scholar 

  • Furukawa, T., Ishii, Y.: Neurophysiological study of hearing in goldfish. J. Neurophysiol.30, 1377–1403 (1967)

    Google Scholar 

  • Görner, P.: The importance of the lateral line system for the perception of surface waves in the clawed toad,Xenopus laevis. Experientia29, 295–296 (1973)

    Google Scholar 

  • Harris, G.G., Van Bergeijk, W.A.: Evidence that the lateral line organ responses to near-field displacements of sound sources in water. J. Acoust. Soc. Amer.34, 1831–1841 (1962)

    Google Scholar 

  • Harris, G.G., Milne, D.C.: Input-output characteristics of the lateral line sense organs ofXenopus. J. Acoust. Soc. Amer.40, 32–42 (1966)

    Google Scholar 

  • Herrick, C.J.: The cranial and first spinal nerves ofMenidia. J. comp. Neurol.2, 153 (1909)

    Google Scholar 

  • Herrick, C.J.: The brain of the Tiger Salamander. Chicago: University Press 1948

    Google Scholar 

  • Hillman, D.E.: Light and electron microscopical study of the relationship between the cerebellum and the vestibular organ of the frog. Exp. Brain Res.9, 1–15 (1969)

    Google Scholar 

  • Kotchabhakdi, N.: Functional circuitry of the goldfish cerebellum. J. comp. Physiol.112, 47–73 (1976)

    Google Scholar 

  • Larsell, O.: The development of the cerebellum in the frogHyla regilla in relation to the vestibular and lateral line systems. J. comp. Neurol.39, 249–289 (1936)

    Google Scholar 

  • Larsell, O.: The comparative anatomy and histology of the cerebellum from the myxinoids through birds (ed. J. Jansen). University Minnesota, Lund Press 1967

  • Llinás, R.: Cerebellar physiology. In: Frog neurobiology (eds. R. Llinás, W. Precht). Berlin-Heidelberg-New York: Springer 1976

    Google Scholar 

  • Llinś, R., Bloedel, J.R., Hillman, D.E.: Functional characteristics of the neuronal circuitry of the frog cerebellar cortex. J. Neurophysiol.32, 847–870 (1969)

    Google Scholar 

  • Llinás, R., Nicholson, C.: Electrophysiological analysis of alligator cerebellar cortex: A study on dendritic spikes. In: First International Symposium on the Neurobiology of Cerebellar Evolution and Development (ed. R. Llinás). Chicago: American Medical Association 1969

    Google Scholar 

  • Llinás, R., Precht, W.: The inhibitory cerebellar efferent system and its relation to the cerebellum in the frog. Exp. Brain Res.9, 16–29 (1969)

    Google Scholar 

  • Llinás, R., Precht, W., Kitai, S.T.: Cerebellar Purkinje cell projection to peripheral vestibular organ in the frog. Science158, 1328–1330 (1967)

    Google Scholar 

  • Magherini, P.C., Giretti, M.L., Precht, W.: Cerebellar control of vestibular neurones of the frog. Pflügers Arch.356, 99–109 (1975)

    Google Scholar 

  • Maler, L.: The acoustico-lateral area of bony fish and its cerebellar relations. Brain. Behav. Evol.10, 130–145 (1974). Also in: Eight nerve systems in vertebrates other than mammals. Basel: S. Karger Publ. 1974

    Google Scholar 

  • McCreery, D.B.: Two types of electroreceptive lateral lemniscal neurones of the lateral line lobe of the catfishIctalurus nebulosus; connections from the lateral line nerve and steady state frequency responses. J. comp. Physiol.113, 317–339 (1977)

    Google Scholar 

  • Nicholson, C., Llinás, R., Precht, W.: Neural elements of the cerebellum of elasmobranch fishes, structural and functional characteristics. In: First International Symposium on the Neurobiology of Cerebellar Evolution and Development (ed. R. Llinás). Chicago: American Medical Association 1969

    Google Scholar 

  • Parvulescu, A.: The acoustics of small tanks. In: Marine bioacoustics, Vol. 2 (ed. W.N. Tavolga). Oxford: Pergamon Press 1967

    Google Scholar 

  • Paul, D.H., Roberts, B.L.: Studies on a primitive cerebellar cortex. 1. The anatomy of the lateral line lobe of the dogfishScyliorhinus. Proc. Roy. Soc. B195, 453–466 (1977a)

    Google Scholar 

  • Paul, D.H., Roberts, B.L.: Studies on a primitive cerebellar cortex. 2. The projections of the posterior lateral line nerve to the lateral line lobe of the dogfish brain. Proc. Roy. Soc. B195, 467–478 (1977b)

    Google Scholar 

  • Paul, D.H., Roberts, B.L.: Studies on a primitive cerebellar cortex. 3. The projection of the anterior lateral line nerve to the lateral line lobes of the dogfish brain. Proc. Roy. Soc. B195, 479–496 (1977c)

    Google Scholar 

  • Pearson, A.A.: The acousticolateral nervous system in fishes. J. comp. Neurol.64, 235–273 (1936a)

    Google Scholar 

  • Pearson, A.A.: The acousticolateral centres and the cerebellum with fibre connections of fishes. J. comp. Neurol.65, 201–294 (1936b)

    Google Scholar 

  • Popper, A.N., Salmon, M., Parvulescu, A.: Sound localisation by Hawaiian squirrelfishes. Anim. Behav.21, 86–97 (1973)

    Google Scholar 

  • Ramón-Moliner, E.: The Golgi-Cox technique. In: Contemporary research methods in neuroanatomy (eds. V.J.H. Nauta, S.O.E. Ebbeson). Berlin-Heidelberg-New York: Springer 1970

    Google Scholar 

  • Rushmer, D.S., Woodward, D.J.: Inhibition of Purkinje cells in the frog cerebellum. 1. Evidence for a stellate cell inhibitory pathway. Brain Res.33, 83–90 (1971)

    Google Scholar 

  • Russell, I.J.: Central and peripheral inhibition of lateral line input during the startle response in the goldfish. Brain Res.80, 517–522 (1974)

    Google Scholar 

  • Russell, I.J.: Amphibian lateral line receptors. In: Frog neurobiology (eds. R. Llinás, W. Precht). Berlin-Heidelberg-New York: Springer 1976a

    Google Scholar 

  • Russell, I.J.: Central inhibition of lateral line input in the medulla of the goldfish by neurones which control active body movements. J. comp. Physiol.111, 335–358 (1976b)

    Google Scholar 

  • Scheich, H., Bullock, T.H., Hamstra, R.J., Jr.: Coding properties of two classes of afferent nerve fibres: High frequency electroreceptors in the electric fishEigenmannia. J. Neurophysiol.36, 39–60 (1973)

    Google Scholar 

  • Schwartz, E.: Lateral line mechanoreceptors in fishes and amphibians. In: Handbook of sensory physiology, Vol. III/3 (ed. A. Fessard), pp. 257–270. Berlin-Heidelberg-New York: Springer 1974

    Google Scholar 

  • Schwartz, E., Hasler, A.D.: Perception of surface waves by the blackstripe Topminnow,Fundulus notatus. J. Fish Res. Bd. Canada23, 1331–1552 (1966)

    Google Scholar 

  • Shimono, T.: Inhibitory mechanism in frog cerebellar cortex. A. Analysis of field potentials. Jap. J. Physiol.23, 381–400 (1973)

    Google Scholar 

  • Strelioff, D., Honruba, V.: Neural transduction inXenopus laevis lateral line system. J. Neurophysiol.41, 432–444 (1978)

    Google Scholar 

  • Tavolga, W.N.: Mechanisms for directional hearing in the sea catfish (Arius felis). J. exp. Biol.67, 97–115 (1977)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This work was supported by a Science Research Council Research Studentship and a Royal Society European Exchange Programme Fellowship. I would like to thank Dr. I.J. Russell for his help and advice throughout this study and Dr. T. Szabo for the invitation to join his group at Gif sur Yvette. Some of the work reported here was submitted to the University of Sussex as partial fulfilment for the requirements of a DPhil degree.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Caird, D.M. A simple cerebellar system: The lateral line lobe of the goldfish. J. Comp. Physiol. 127, 61–74 (1978). https://doi.org/10.1007/BF00611926

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00611926

Keywords

Navigation