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Divergent axon collaterals from rat cerebellar nuclei to diencephalon, mesencephalon, medulla oblongata and cervical cord

A fluorescent double retrograde labeling study

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The existence of divergent axon collaterals of neurons in the deep cerebellar nuclei has been investigated in rat by means of the fluorescent retrograde double labeling technique. The results have led to the following conclusions.

  1. A.

    Many of the neurons in the lateral, the interpositus as well as the caudal half of the medial nucleus project to the diencephalon. Some of these neurons distribute divergent axon collaterals to the superior colliculus, but few neurons project only to the latter structure.

  2. B.

    Some of the deep cerebellar neurons located laterally, i.e. in the dorsomedial part of the lateral nucleus, as well as some others located medially, i. e. in the medial part of the interpositus nucleus and the adjoining part of the medial nucleus, distribute divergent axon collaterals to the diencephalon and the spinal cord.

  3. C.

    Deep cerebellar neurons located laterally: in the cell group of the dorsolateral hump (Dlh) and in the adjoining lateral part of the interpositus nucleus, as well as some others located medially, i.e. in the dorsolateral part of the medial nucleus (Mdlp), distribute divergent axon collaterals to the diencephalon and to the medulla oblongata, probably primarily its medial reticular formation. However, only few of the neurons, which distribute descending collaterals to the spinal cord or the medulla oblongata, distribute ascending collaterals to the superior colliculus.

  4. D.

    After injections in the medulla oblongata a population of small sized single labeled neurons was encountered especially in the lateral and interpositus nuclei. On the basis of other findings in rat they were assumed to represent cerebello-olivary neurons.

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  1. Achenbach KE, Goodman DC (1968) Cerebellar projections to pons, medulla and spinal cord in the albino rat. Brain Behav Evol 1: 43–57

  2. Angaut P, Bowsher D (1970) Ascending projections of the medial cerebellar (fastigial) nucleus: An experimental study in the cat. Brain Res 24: 49–68

  3. Asanuma C, Thach WT, Jones EG (1980) Nucleus interpositus projection to spinal interneurons in monkeys. Brain Res 191: 245–248

  4. Ban M, Ohno T (1977) Projection of cerebellar nuclear neurones to the inferior olive by descending collaterals of ascending fibres. Brain Res 133: 155–161

  5. Batton RR, Jayaraman A, Ruggiero D, Carpenter MB (1977) Fastigial efferent projections in the monkey: An autoradiographic study. J Comp Neurol 174: 281–306

  6. Beitz AJ, Chan Palay V (1979a) The medial cerebellar nucleus in the rat: Nuclear volume, cell number, density and orientation. Neuroscience 4: 31–45

  7. Beitz AJ, Chan Palay V (1979b) A Golgi analysis of neuronal organization in the medial cerebellar nucleus of the rat. Neuroscience 4: 47–63

  8. Bentivoglio M, Kuypers HGJM, Catsman-Berrevoets CE (1980a) Retrograde neuronal labeling by means of bisbenzimide and nuclear yellow (Hoechst S769121). Measures to prevent diffusion of the tracers out of retrogradely labeled neurons. Neurosci Lett 18: 19–24

  9. Bentivoglio M, Kuypers HGJM, Catsman-Berrevoets CE, Dann O (1979a) Fluorescent retrograde neuronal labeling in rat by means of substances binding specifically to adenine-thymine rich DNA. Neurosci Lett 12: 235–240

  10. Bentivoglio M, Kuypers HGJM, Catsman-Berrevoets CE, Loewe H, Dann O (1980b) Two new fluorescent retrograde neuronal tracers which are transported over long distances. Neurosci Lett 18: 25–30

  11. Bentivoglio M, van der Kooy D, Kuypers HGJM (1979b) The organization of the efferent projections of the substantia nigra in the rat. A retrograde fluorescent double labeling study. Brain Res 174: 1–17

  12. Bharos TB, Kuypers HGJM, Lemon RN, Muir RB (1981) Divergent collaterals from deep cerebellar neurons to thalamus and tectum, and to medulla oblongata and spinal cord: Retrograde fluorescent and electrophysiological studies. Exp Brain Res 42: 399–410

  13. Brown JT, Chan Palay V, Palay SL (1977) A study of afferent input to the inferior olivary complex in the rat by retrograde axonal transport of horseradish peroxidase. J Comp Neurol 176: 1–22

  14. Buisseret Delmas C, Batini C (1978) Topology of the pathways to the inferior olive: An HRP study in cat. Neurosci Lett 10: 207–214

  15. Cajal SR (1972) Histologie du systéme nerveux. Institute Ramón y Cajal, Madrid

  16. Carpenter MB (1959) Lesions of the fastigial nuclei in the rhesus monkey. Am J Anat 104: 1–33

  17. Carpenter MB, Stevens GH (1957) Structural and functional relationships between the deep cerebellar nuclei and the brachium conjunctivum in the rhesus monkey. J Comp Neurol 107: 109–163

  18. Castro AJ (1978) Projections of the superior cerebellar peduncle in rats and the development of new connections in response to neonatal hemicerebellectomy. J Comp Neurol 178: 611–628

  19. Catsman-Berrevoets CE, Lemon RN, Verburgh CA, Bentivoglio M, Kuypers HGJM (1980) Absence of callosal collaterals derived from rat corticospinal neurons. A study using fluorescent retrograde tracing and electrophysiological techniques. Exp Brain Res 39: 433–440

  20. Caughell KA, Flumerfelt BA (1977) The organization of the cerebellorubral projection: An experimental study in the rat. J Comp Neurol 176: 295–306

  21. Chan Palay V (1977) Cerebellar dentate nucleus: organization, cytology and transmitters. Springer, Berlin Heidelberg New York

  22. Cohen D, Chambers WW, Sprague JM (1958) Experimental study of the efferent projections from the cerebellar nuclei to the brainstem of the cat. J Comp Neurol 109: 233–259

  23. Deniau JM, Hammond C, Riszk A, Feger J (1978) Electrophysiological properties of identified output neurons of the rat substantia nigra (pars compacta and pars reticulata): Evidences for the existence of branched neurons. Exp Brain Res 32: 409–422

  24. Dietrichs E, Walberg F (1981) The cerebellar nucleo-olivary projection in the cat. Anat Embryol 162: 51–67

  25. Dom R, King JS, Martin GF (1973) Evidence for two direct cerebello-olivary connections. Brain Res 57: 498–501

  26. Faull RLM (1978) The cerebellofugal projections in the brachium conjunctivum of the rat. II. The ipsilateral and contralateral descending pathways. J Comp Neurol 178: 519–536

  27. Faull RLM, Carman JB (1978) The cerebellofugal projections in the brachium conjunctivum of the rat. I. The contralateral ascending pathway. J Comp Neurol 178: 495–518

  28. Flood S, Jansen J (1966) The efferent fibres of the cerebellar nuclei and their distribution on the cerebellar peduncles in the cat. Acta Anat 63: 137–166

  29. Fukushima K, Peterson BW, Uchino Y, Coulter JD, Wilson VJ (1977) Direct fastigiospinal fibers in the cat. Brain Res 126: 538–542

  30. Gould BB, Graybiel AM (1976) Afferents to the cerebellar cortex in the cat: Evidence for an intrinsic pathway leading from the deep nuclei to the cortex. Brain Res 110: 601–611

  31. Graybiel AM, Nauta HJW, Lasek RJ, Nauta WJH (1973) A cerebello-olivary pathway in the cat: An experimental study using autoradiography tracing techniques. Brain Res 58: 205–211

  32. Haroian AJ, Massopust LC, Young PA (1981) Cerebellothalamic projections in the rat: An autoradiographic and degeneration study. J Comp Neurol 197: 217–236

  33. Hendry SHC, Jones EG, Graham J (1979) Thalamic relay nuclei for cerebellar and certain related fiber systems in the cat. J Comp Neurol 185: 679–714

  34. Huisman AM, Kuypers HGJM, Verburgh CA (1981) Quantitative differences in collateralisation of the descending spinal pathways from red nucleus and other brain stem cell groups in rat as demonstrated with the multiple fluorescent retrograde tracer technique. Brain Res 209: 271–286

  35. Jansen J, Jansen J (1955) On the efferent fibers of the cerebellar nuclei in the cat. J Comp Neurol 102: 607–632

  36. Kalil K (1979) Projections of the cerebellar and dorsal column nuclei upon the inferior olive in the rhesus monkey: An autoradiographic study. J Comp Neurol 188: 43–62

  37. Kievit J (1979) Cerebello-talamische projecties en de afferente verbindingen naar de frontale schors in the rhesus aap. Thesis, Rotterdam Medical School, Bronder-Offset, Rotterdam

  38. Kievit J, Kuypers HGJM (1972) Fastigial cerebellar projections to the ventrolateral nucleus of the thalamus and the organization of the descending pathways. In: Frigyesi T, Rinvik E, Yahr MD (eds) Corticothalamic projections and sensorimotor activities. Raven Press, New York, pp 91–114

  39. Korneliussen HK (1968) On the morphology and subdivision of the cerebellar nuclei of the rat. J Hirnforsch 10: 109–122

  40. Kuypers HGJM, Catsman-Berrevoets CE, Padt RE (1977) Retrograde axonal transport of fluorescent substances in the rat's forebrain. Neurosci Lett 6: 127–135

  41. Kuypers HGJM, Bentivoglio M, van der Kooy D, Catsman-Berrevoets CE (1979) Retrograde transport of bisbenzimide and propidium iodide through axons to their parent bodies. Neurosci Lett 12: 1–7

  42. Kuypers HGJM, Bentivoglio M, Catsman-Berrevoets CE, Bharos TP (1980) Double retrograde neuronal labeling through divergent axon collaterals, using two fluorescent tracers with the same excitation wavelength which label different features of the cell. Exp Brain Res 40: 383–392

  43. Malmgren L, Olsson Y (1978) A sensitive method for histochemical demonstration of horseradish peroxidase in neurons following retrograde axonal transport. Brain Res 148: 279–294

  44. Martin GF, Henkel CK, King JS (1976) Cerebello-olivary fibers: their origin, course and distribution in the North American opossum. Exp Brain Res 24: 219–236

  45. Martin GF, King JS, Dom R (1974) The projections of the deep cerebellar nuclei of the opossum, Didelphis marsupialis virginians. J Hirnforsch 15: 545–573

  46. Matsushita M, Hosoya Y (1978) The location of spinal projection neurons in the cerebellar nuclei (cerebellospinal tract neurons) of the cat. A study with the horseradish peroxidase technique. Brain Res 142: 237–248

  47. McCrea RA, Bishop GA, Kitai ST (1978) Morphological and electrophysiological characteristics of projection neurons in the nucleus interpositus of the cat cerebellum. J Comp Neurol 181: 397–420

  48. Nakano K, Takimoto T, Kayahara T, Takeuchi Y, Kobayashi Y (1980) Distribution of cerebellothalamic neurons projecting to the ventral nuclei of the thalamus: An HRP study in the cat. J Comp Neurol 194: 427–439

  49. Rand RW (1954) An anatomical and experimental study of the cerebellar nuclei and their efferent pathways in the monkey. J Comp Neurol 101: 167–223

  50. Rosina A, Provini L, Bentivoglio M, Kuypers HGJM (1980) Ponto-neocerebellar axonal branching as revealed by double fluorescent retrograde labeling technique. Brain Res 195: 461–466

  51. Stanton GB (1980) Topographical organization of ascending cerebellar projections from the dentate and interposed nuclei in Macaca mulatta: An anterograde degeneration study. J Comp Neurol 190: 699–731

  52. Steindler DA, Deniau JM (1980) Anatomical evidence for collateral branching of substantia nigra neurons: A combined horseradish peroxidase and 3H-wheat germ agglutinin axonal transport study in the rat. Brain Res 196: 228–236

  53. Sugimoto T, Mizuno N, Itoh K (1981) An autoradiographic study on the terminal distribution of cerebellothalamic fibres in the cat. Brain Res 215: 29–47

  54. Sugimoto T, Mizuno N, Nomura S, Nakamura Y (1980) Fastigioolivary fibers in the cat as revealed by the autoradiographic tracing method. Brain Res 199: 443–446

  55. Thach WT, Jones EG (1979) The cerebellar dentatothalamic connection: Terminal field, lamellae, rods and somatotopy. Brain Res 169: 168–172

  56. Thomas DM, Kaufman RP, Sprague JM, Chambers WW (1956) Experimental studies of the vermal cerebellar projections in the brain stem of the cat (fastigiobulbar tract). J Anat (Lond) 90: 371–385

  57. Tolbert DL, Bantli H, Bloedel JR (1976a) Anatomical and physiological evidence for a cerebellar nucleo-cortical projection in the cat. Neuroscience 1: 205–217

  58. Tolbert DL, Bantli H, Bloedel JR (1978) Multiple branching of cerebellar efferent projections in cats. Exp Brain Res 31: 305–316

  59. Tolbert DL, Massopust LC, Murphy MC, Young PA (1976b) The anatomical organization of the cerebello-olivary projection in the cat. J Comp Neurol 170: 525–544

  60. van der Kooy D, Kuypers HGJM, Catsman-Berrevoets CE (1978) Single mammillary body cells with divergent axon collaterals. Demonstration by a simple, fluorescent retrograde double labeling technique in the rat. Brain Res 158: 189–196

  61. Voogd J (1964) The Cerebellum of the Cat. Structure and fiber connexions. Thesis, Van Gorcum & Co., Assen

  62. Walberg F, Pompeiano O, Brodal A, Jansen J (1962) The fastigiovestibular projection in the cat. An experimental study with silver impregnation methods. J Comp Neurol 118: 49–75

  63. Ware CB, Mufson EJ (1979) Spinal cord projections from the medial cerebellar nucleus in tree shrew (Tupaia glis). Brain Res 171: 383–400

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Correspondence to Dr. M. Bentivoglio.

Additional information

Supported in part by Grant 134691 of the FUNGO/ZWO (Dutch Organization for Fundamental Research in Medicine) and Grant 80.00515.04 of the CNR (Italian National Research Council)

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Bentivoglio, M., Kuypers, H.G.J.M. Divergent axon collaterals from rat cerebellar nuclei to diencephalon, mesencephalon, medulla oblongata and cervical cord. Exp Brain Res 46, 339–356 (1982). https://doi.org/10.1007/BF00238629

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Key words

  • Cerebellar nuclei
  • Axon collaterals
  • Cerebellar efferents
  • Double labeling
  • Fluorescent tracers