Skip to main content
Log in

The fine structure of neurones and cellular relationships in the abducens nucleus in the cat

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

Light and electron microscope studies of the abducens nucleus in the cat have disclosed two populations of neurones: large neurones 25 to 75 μm in diameter and small neurones 10 to 25 μm in diameter. Characteristic of the large neurones are a highly developed granular endoplasmic reticulum and a large number of axo-somatic synapses. The small neurones have a poorly developed granular endoplasmic reticulum and comparative by few axo-somatic synapses.

Injection of horseradish peroxidase (HRP) into the ipsilateral lateral rectus muscle has been used to identify abducens motoneurones which represent 65% of the total number of cells in the abducens nucleus and form part of the large cell population. The remaining unlabelled large neurones (30% of the large cell population) probably represent motoneurones of the retractor bulbi muscles, abducens motoneurones which have failed to transport the HRP, and possibly internuclear neurones. The small neurones (5% of the total cell population) were never labelled by HRP.

Axo-somatic and axo-dendritic synapses are numerous. Many of the synaptic terminals form contacts with two or more different postsynaptic elements. Axo-axonic synapses and synapses on the initial segments of large neurones are also present. Nodal synapses and branching of myelinated axons are common findings. Finally, extended areas of close apposition between dendritic membranes are frequently observed.

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

References

  • Alvarado-Mallart, M.R., Batini, C., Buisseret-Delmas, C., Corvisier, J.: Trigeminal representations of the masticatory and extraocular proprioceptors as revealed by horseradish peroxidase retrograde transport. Exp. Brain Res. 23, 167–179 (1975a)

    Google Scholar 

  • Alvarado-Mallart, M.R., Batini, C., Buisseret, C., Gueritaud, J.P., Horcholle-Bossavit, G.: Mesencephalic projections of the reclus lateralis muscle afferents in the cat. Arch. Ital. Biol. 113, 1–20 (1975b)

    Google Scholar 

  • Angaut, P., Sotelo, C.: The fine structure of the cerebellar central nuclei in the cat. II. Synaptic organization. Exp. Brain Res. 16, 431–454 (1973)

    Google Scholar 

  • Bach-y-Rita, P.: Neurophysiology of eye movements. In: The control of eye movements. (P. Bach-y-Rita, C.C. Collins, eds.). pp. 7–45. New York: Academic Press 1971

    Google Scholar 

  • Bak, I.J., Choi, W.B.: Electron microscopic investigation of synaptic organization of the trochlear nucleus in cat. I. Normal ultrastructure. Cell Tiss. Res. 150, 409–423 (1974)

    Google Scholar 

  • Bak, I.J., Baker, R., Choi, W.B., Precht, W.: Electron microscopic investigation of the vestibular projection to the cat trochlear nuclei. Neuroscience 1, 477–482 (1976)

    Google Scholar 

  • Baker, R., Highstein, S.M.: Physiological identification of interneurons and motoneurons in the abducens nucleus. Brain Res. 91, 292–298 (1975)

    Google Scholar 

  • Büttner-Ennever, J.A., Henn, V.: An autoradiographic study of the pathways from the pontine reticular formation involved in horizontal eye movements. Brain Res. 108, 155–164 (1976)

    Google Scholar 

  • Carpenter, M.B.: Human Neuroanatomy. pp. 349–351. Baltimore: Williams and Wilkins 1976

    Google Scholar 

  • Carpenter, M.B., Strominger, N.L.: The medial longitudinal fasciculus and disturbances of conjugate horizontal eye movements in the monkey. J. Comp. Neurol. 125, 41–66 (1965)

    Google Scholar 

  • Clamann, H.P., Henneman, E.: Electrical measurement of axon diameter and its use in relating motoneuron size to critical firing level. J. Neurophysiol. 39, 844–851 (1976)

    Google Scholar 

  • Destombes, J., Ripert, J.P.: Données ultrastructurales sur le noyau abducens chez le chat. J. Microsc. Biol. Cell. 23, 44a-45a (1975)

    Google Scholar 

  • Destombes, J., Ripert, J.P.: Ultrastructural observations of the abducens nucleus of the cat after injection of horseradish peroxidase into the lateral rectus muscle. Exp. Brain Res. 28, 63–71 (1977)

    Google Scholar 

  • Gacek, R.R.: Anatomical demonstration of the vestibulo-ocular projections in the cat. Laryngoscope 81, 1559–1595 (1971)

    Google Scholar 

  • Gacek, R.R.: Localisation of neurons supplying the extraocular muscles in the kitten using horseradish peroxidase. Exp. Neurol. 44, 381–403 (1974)

    Google Scholar 

  • Gacek, R.R.: Location of brain stem neurons projecting to the oculomotor nucleus in the cat. Exp. Neurol. 57, 725–749 (1977)

    Google Scholar 

  • Gogan, P., Gueritaud, J.P., Horcholle-Bossavit, G., Tyć-Dumont, S.: Inhibitory nystagmic interneurons. Physiological and anatomical identification within the abducens nucleus. Brain Res. 59, 410–416 (1973)

    Google Scholar 

  • Gogan, P., Gueritaud, J.P., Horcholle-Bossavit, G., Tyć-Dumont, S.: Electrotonic coupling between motoneurons in the abducens nucleus of the cat. Exp. Brain Res. 21, 139–154 (1974)

    Google Scholar 

  • Gogan, P., Gueritaud, J.P., Horcholle-Bossavit, G., Tyć-Dumont, S.: Direct excitatory interactions between spinal motoneurones of the cat. J. Physiol. (Lond.) 272, 755–767 (1977)

    Google Scholar 

  • Graham, R.C., Karnovsky, M.J.: The early stages of absorption of injected horseradish peroxidase in the proximal tubule of mouse kidney ultrastructural cytochemistry by a new technique. J. Histochem. 14, 291–302 (1966)

    Google Scholar 

  • Grant, K., Gueritaud, J.P., Horcholle-Bossavit, G., Tyć-Dumont, S.: Properties of vestibulo-ocular neurones. In: Control of gaze by brain stem neurons. (R. Baker, A. Berthoz, eds.). pp. 235–242. Amsterdam: Elsevier 1978

    Google Scholar 

  • Gray, E.G.: Axosomatic and axodendritic synapses of the cerebral cortex: an electron microscopic study. J. Anat. 93, 420–433 (1959)

    Google Scholar 

  • Gray, E.G., Guillery, R.W.: Synaptic morphology in the normal and degenerating nervous system. Int. Rev. Cytol. 19, 111–182 (1966)

    Google Scholar 

  • Graybiel, A.M.: Direct and indirect preoculomotor pathways of the brainstem: an autoradiographic study of the pontine reticular formation in the cat. J. Comp. Neurol. 175, 37–78 (1977a)

    Google Scholar 

  • Graybiel, A.M.: Organization pathways in the cat and rhesus monkey. In: Control of gaze by brain stem neurons. (R. Baker, A. Berthoz, eds.). pp. 79–89. Amsterdam: Elsevier 1977b

    Google Scholar 

  • Graybiel, A.W., Hartwieg, E.A.: Some afferent connections of the oculomotor complex in the cat: an experimental study with tracer technique. Brain Res. 81, 543–551 (1974)

    Google Scholar 

  • Grinnell, A.D.: A study of the interaction between motoneurons in the frog spinal cord. J. Physiol. (Lond.) 182, 612–648 (1966)

    Google Scholar 

  • Hámori, J., Mezey, E.: Serial and triadic synapses in the cerebellar nuclei of the cat. Exp. Brain Res. 30, 259–273 (1977)

    Google Scholar 

  • Kerneil, D.: Input resistance, electrical excitability and size of ventral horn cells in cat spinal cord. Science 152, 1637–1640 (1966)

    Google Scholar 

  • Lorente de Nó, R.: Vestibulo-ocular reflex arc. Arch. Neurol. Psychiat. (Chicago) 30, 245–291 (1933)

    Google Scholar 

  • Maciewicz, R.J., Kaneko, C.R.S., Highstein, S.M., Baker, R.: Morphophysiologjcal identification of interneurons in the oculomotor nucleus that project to the abducens nucleus in the cat. Brain Res. 96, 60–65 (1975)

    Google Scholar 

  • Maciewicz, R.J., Spencer, R.F.: Oculomotor and abducens internuclear pathways in the cat. In: Control of gaze by brain stem neurons. (R. Baker, A. Berthoz, eds.). pp. 99–108. Amsterdam: Elsevier 1977

    Google Scholar 

  • Magherini, P.C.: Evidence for electrotonic coupling between frog motoneurons in the in situ spinal cord. J. Neurophysiol. 39, 474–483 (1976)

    Google Scholar 

  • Matthews, M.A., Willis, W.D., Williams, V.: Dendrites bundles in lamina IX of cat spinal cord: a possible source for electrical interaction between motoneurons? Anat. Rec. 171, 313–328 (1971)

    Google Scholar 

  • Mugnaini, E., Walberg, F., Hauglie-Hanssen, E.: Observations on the fine structure of the lateral vestibular nucleus (Deiter's nucleus) in the cat. Exp. Brain Res. 4, 146–186 (1967)

    Google Scholar 

  • Nelson, P.G.: Interaction between spinal motoneurons of the cat. J. Neurophysiol. 29, 275–287 (1966)

    Google Scholar 

  • Pappas, G.D., Cohen, E.B., Purpura, D.P.: Fine structure of synaptic and non-synaptic neuronal relations in the thalamus of the cat. In: The Thalamus. (D.P. Purpura, M.D. Yahr, eds.). pp. 47–75. New York: Columbia University Press 1966

    Google Scholar 

  • Peters, A., Palay, S.L., Webster, H.F. de: The fine structure of the nervous system. The neurons and supporting cells. Philadelphia: Saunders 1976

    Google Scholar 

  • Rall, W.: Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J. Neurophysiol. 30, 1138–1168 (1967)

    Google Scholar 

  • Rall, W., Burke, R.E., Smith, T.G., Nelson, P.G., Frank, K.: Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. J. Neurophysiol. 30, 1169–1193 (1967)

    Google Scholar 

  • Ramón-y-Cajal, S.: Histologie du système nerveux de l'homme et des vertébrés. Paris: Maloine 1909–1911

    Google Scholar 

  • Schmitt, F.O., Dev, P., Smith, B.H.: Electrotonic processing of information by brain cells. Science 193, 114–120 (1976)

    Google Scholar 

  • Sonnhof, U., Richter, D.W., Taugner, R.: Electrotonic coupling between frog spinal motoneurons. An electrophysiological and morphological study. Brain Res. 138, 197–215 (1977)

    Google Scholar 

  • Somogyi, P., Hámori, J.: A quantitative electron microscopic study of the Purkinje cell axon initial segment. Neuroscience 1, 361–365 (1976)

    Google Scholar 

  • Sotelo, C.: Morphological correlates of electrotonic coupling between neurons in mammalian nervous system. In: Golgi centennial Symposium. (M. Santini, ed.). pp. 355–365. New York: Raven Press 1975

    Google Scholar 

  • Sotelo, C., Palay, S.L.: The fine structure of the lateral vestibular nucleus in the rat. I. Neurons and neuroglial cells. J. Cell Biol. 36, 151–179 (1968)

    Google Scholar 

  • Sotelo, C., Taxi, J.: Ultrastructural aspects of electrotonic junctions in the spinal cord of the frog. Brain Res. 17, 137–141 (1970)

    Google Scholar 

  • Spencer, R.F., Sterling, P.: An electron microscope study of motoneurones and interneurones in the cat abducens nucleus identified by retrograde intraaxonal transport of horseradish peroxidase. J. Comp. Neurol. 176, 65–85 (1977)

    Google Scholar 

  • Steiger, H.D., Büttner-Ennever, J.A.: Relationship between motoneurons and interneurons in the abducens nucleus: a double retrograde tracer study in the cat. Brain Res. 148, 181–188 (1978)

    Google Scholar 

  • Steinacker, A., Bach-y-Rita, P.: The fiber spectrum of the cat VI nerve to the lateral rectus and retractor bulbi muscles. Experientia 24, 1254–1255 (1968)

    Google Scholar 

  • Stensaas, L.J., Stensaas, S.S.: Light and electron microscopy of motoneurons and neuropil in the amphibian spinal cord. Brain Res. 31, 67–84 (1971)

    Google Scholar 

  • Sterling, P.: Anatomy and physiology of goldfish oculomotor system. I. Structure of abducens nucleus. J. Neurophysiol. 40, 557–572 (1977)

    Google Scholar 

  • Székely, G., Kosaras, B.: Dendro-dendritic contacts between frog motoneurons shown with the cobalt labelling technique. Brain Res. 108, 194–198 (1976)

    Google Scholar 

  • Szentágothai, J.: Pathways and synaptic articulation patterns connecting vestibular receptors and oculomotor nuclei. In: The oculomotor system. (M.B. Bender, ed.). p. 205. New York: Harper and Row 1964

    Google Scholar 

  • Szentágothai, J., Arbib, M.A.: In conceptual models of neurol organization. Neurosci. Res. Progr. Bull. 12, 399 (1974)

    Google Scholar 

  • Tarlov, E.: Organization of vestibulo-oculomotor projections in the cat. Brain Res. 20, 159–179 (1970)

    Google Scholar 

  • Tredici, G., Pizzini, G., Milanesi, S.: The ultrastructure of the nucleus of the oculomotor nerve (somatic efferent portion) of the cat. Anat. Embryol. (Berl.) 149, 323–346 (1976)

    Google Scholar 

  • Van Gehuchten, A.: Quoted in Traité d'Anatomie Humaine. (L. Testut, A. Latarjet, eds.). p. 130. Paris: Doin 1949

    Google Scholar 

  • Van Gebuchten, A.: Recherche sur l'origine réelle des nerfs crâniens: I. Les nerfs moteurs oculaires. J. Neurol. Hypnol. 3, 114–129 (1898)

    Google Scholar 

  • Warwick, R.: Representation of the extra-ocular muscles in the oculomotor nuclei of the monkey. J. Comp. Neurol. 98, 449–504 (1953)

    Google Scholar 

  • Warwick, R.: Oculomotor organization. In: The oculomotor system (M.B. Bender, ed.). pp. 173–204. New York: Harper and Row 1964

    Google Scholar 

  • Washizu, Y.: Single spinal motoneurons excitable from two different antidromic pathways. Jpn. J. Physiol. 10, 121–131 (1960)

    Google Scholar 

  • Waxman, S.G.: An ultrastructural study of the pattern of myelination of preterminal fibers in teleost oculomotor nuclei, electromotor nuclei and spinal cord. Brain Res. 27, 189–201 (1971)

    Google Scholar 

  • Waxman, S.G.: Regional differentiation of the axon: a review with special reference to the concept of the multiplex neuron. Brain Res. 47, 269–288 (1972)

    Google Scholar 

  • Waxman, S.G., Pappas, G.D.: An electron microscopic study of synaptic morphology in the oculomotor nuclei of three infra-mammalian species. J. Comp. Neurol. 143, 41–72 (1971)

    Google Scholar 

  • Werman, R., Carlen, P.L.: Unusual behavior of the Ia EPSP in cat spinal motoneurons. Brain Res. 112, 395–401 (1976)

    Google Scholar 

  • Wong-Riley, M.T.T.: Endogenous peroxidatic activity in brain stem neurons as demonstrated by their staining with diaminobenzidine in normal squirrel monkeys. Brain Res. 108, 257–277 (1976)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported by INSERM (U6), CNRS (GR 25) and grant RCP 391 from the CNRS

Rights and permissions

Reprints and permissions

About this article

Cite this article

Destombes, J., Gogan, P. & Rouvière, A. The fine structure of neurones and cellular relationships in the abducens nucleus in the cat. Exp Brain Res 35, 249–267 (1979). https://doi.org/10.1007/BF00236614

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00236614

Key words

Navigation