Experimental Brain Research

, Volume 65, Issue 1, pp 200–212 | Cite as

The cerebellotectal pathway in the grey squirrel

  • P. J. May
  • W. C. Hall
Regular Papers


In the well laminated superior colliculus of the grey squirrel the cells of origin of the crossed descending pathway to the brainstem gaze centers are contained within the inner sublamina of the intermediate grey layer. The technique of anterograde transport of horseradish peroxidase was used to determine whether the pathway from the cerebellum to the superior colliculus terminates in this region. The technique of retrograde transport of horseradish peroxidase was used to localize the source of this pathway within the cerebellum and to determine the morphology of the cerebellotectal neurons. The grey squirrel cerebellotectal pathway provides two terminal fields to the superior colliculus: a diffuse projection into the deep grey layer and a more concentrated, interrupted projection into the inner sublamina of the intermediate grey layer. The more concentrated projection overlies precisely the tectal sublamina that contains the cells of origin of the predorsal bundle. In contrast to animals with frontal eyes, the cerebellotectal pathway in the grey squirrel was found to project almost entirely contralaterally and the vast majority of the cells of origin for the pathway were distributed ventrally, in the caudal pole of the posterior interpositus nucleus and the adjacent region of the dentate. The labelled cells in both cerebellar nuclei were large and displayed similar morphologies.

Key words

Superior colliculus Cerebellum Deep cerebellar nuclei Predorsal bundle Deep tectal layers 



Brachium conjunctivum


Brachium pontis


Cochlear nuclei


Dentate nucleus of the cerebellum


Dorsal lateral geniculate nucleus


Dorsal lateral pontine grey


Interpositus nucleus of the cerebellum


Inferior colliculus


Oculomotor nucleus


Inferior olive


Ipsilateral tectobulbar pathway


Fastigial nucleus of the cerebellum


Medial geniculate nucleus


Nucleus reticularis tegmenti pontis


Stratum opticum


Periaqueductal grey


Predorsal bundle


Parabigeminal nucleus


Prepositus hypoglossi


Pulvinar nucleus




Red nucleus


Stratum album intermediale (intermediate white layer)


Stratum album profundum (deep white layer)


Stratum griseum intermediale (intermediate grey layer)


Stratum griseum profundum (deep grey layer)


Stratum griseum superficiale (superficial grey layer)


Substantia nigra


Sensory division of the trigeminal complex


Vestibular nuclei


Facial nucleus


Ventral lateral geniculate nucleus


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  1. Angaut P (1969) The fastigio-tectal projections. An anatomical experimental study. Brain Res 13: 186–189Google Scholar
  2. Araki M, McGeer PL, McGeer EG (1984) Presumptive gamma-aminobutyric acid pathways from the midbrain to the superior colliculus studied by a combined horseradish peroxidase gamma-aminobutyric acid transaminase pharmacohistochemical method. Neuroscience 13: 433–439Google Scholar
  3. Ariens Kappers CU, Huber GC, Crosby EC (1967) The comparative anatomy of the nervous system of vertebrates including man. Hafner Pub Co, New York, Vol II, pp 1239Google Scholar
  4. Armstrong DM, Schild RF (1978A) An investigation of the cerebellar corticonuclear projections in the rat using an autoradiographic tracing method. I. Projections from the vermis. Brain Res 141: 1–19Google Scholar
  5. Armstrong DM, Schild RF (1978B) An investigation of the cerebellar cortico-nuclear projections in the rat using an autoradiographic tracing method. II. Projections from the hemisphere. Brain Res 141: 235–249Google Scholar
  6. Batton RRI, Jayaraman A, Ruggiero D, Carpenter MB (1977) Fastigial efferent projections in the monkey: an autoradiographic study. J Comp Neurol 174: 281–306Google Scholar
  7. Chan-Palay V (1977) Cerebellar dentate nucleus: organization, cytology and transmitters. Springer, Berlin Heidelberg New York, pp 297–363Google Scholar
  8. Chevalier G, Deniau JM (1982) Inhibitory nigral influence on cerebellar evoked responses in the rat ventromedial thalamic nucleus. Exp Brain Res 48: 369–376Google Scholar
  9. Chevalier G, Vacher JM, Deniau JM, Desban M (1985) Disinhibition as a basic process in the expression of striatal functions. I. The striato-nigral influence on tecto-spinal/tecto-diencephalic neurons. Brain Res 334: 215–226Google Scholar
  10. Courville J, Diakiw N (1976) Cerebellar corticonuclear projection in the cat. The vermis of the anterior and posterior lobes. Brain Res 110: 1–20Google Scholar
  11. Earle AM, Matzke HA (1974) Efferent fibers of the deep cerebellar nuclei in hedgehogs. J Comp Neurol 154: 117–132Google Scholar
  12. Faull RL, Carman JB (1978) The cerebellofugal projections in the brachium conjunctivum of the rat. I. The contralateral ascending pathway. J Comp Neurol 178: 495–518Google Scholar
  13. Flood S, Jansen J (1961) On the cerebellar nuclei in the cat. Acta Anat 46: 52–72Google Scholar
  14. Frankfurter A, Weber JT, Harting JK (1977) Brain stem projections to lobule VII of the posterior vermis in the squirrel monkey, as demonstrated by the retrograde axonal transport of tritiated horseradish peroxidase. Brain Res 124: 135–139Google Scholar
  15. Frankfurter A, Weber JT, Royce GJ, Strominger NL, Harting JK (1976) An autoradiographic analysis of the tecto-olivary projection in primates. Brain Res 118: 245–257Google Scholar
  16. Grantyn A, Grantyn R, Robine KP, Berthoz A (1979) Electroanatomy of tectal efferent connections related to eye movements in the horizontal plane. Exp Brain Res 37: 149–172Google Scholar
  17. Graybiel AM (1975) Anatomical organization of retinotectal afferents in the cat: an autoradiographic study. Brain Res 96: 1–23Google Scholar
  18. Graybiel AM (1978) Organization of the nigrotectal connection: an experimental tracer study in the cat. Brain Res 143: 339–348Google Scholar
  19. Hall WC, May PJ (1984) The anatomical basis for sensorimotor transformations in the superior colliculus. In: Neff WD (ed) Contributions to sensory physiology, Vol 8. Academic Press, San Diego, pp 1–40Google Scholar
  20. Henkel CK, Edwards SB (1978) The superior colliculus control of pinna movements in the cat: possible anatomical connections. J Comp Neurol 182: 763–776Google Scholar
  21. Hepp K, Henn V, Jaeger J (1982) Eye movement related neurons in the cerebellar nuclei of the alert monkey. Exp Brain Res 45: 253–264Google Scholar
  22. Hirai T, Onodera S, Kawamura K (1982) Cerebellotectal projections studied in cats with horseradish peroxidase or tritiated amino acids axonal transport. Exp Brain Res 48: 1–12Google Scholar
  23. Hikosaka O, Wurtz RH (1985) Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus. J Neurophysiol 53: 266–291Google Scholar
  24. Hoddevik GH, Brodal A, Walberg F (1976) The olivocerebellar projection in the cat studied with the method of retrograde axonal transport of horseradish peroxidase. II. The projection of the vermal visual area. J Comp Neurol 169: 155–170Google Scholar
  25. Holcombe V, Hall WC (1981A) Laminar origin of ipsilateral tectopontine pathways. Neuroscience 6: 255–260Google Scholar
  26. Holcombe V, Hall WC (1981B) The laminar origin and distribution of the crossed tectoreticular pathways. J Neurosci 10: 1103–1112Google Scholar
  27. Huerta MF, Harting JK (1982) Tectal control of spinal cord activity: neuroanatomical demonstration of pathways connecting the superior colliculus with the cervical spinal cord grey. Prog Brain Res 57: 293–328Google Scholar
  28. Kalil K (1981) Projections of the cerebellar and dorsal column nuclei upon the thalamus of the rhesus monkey. J Comp Neurol 195: 25–50Google Scholar
  29. Kase M, Miller DC, Noda H (1980) Discharges of Purkinje cells and mossy fibres in the cerebellar vermis of the monkey during saccadic eye movements and fixation. J Physiol 300: 539–555Google Scholar
  30. Kawamura K, Brodal A (1973) The tectopontine projection in the cat: an experimental anatomical study with comments on pathways for teleceptive impulses to the cerebellum. J Comp Neurol 149: 371–390Google Scholar
  31. Kawamura K, Hashikawa T (1979) Olivocerebellar projections in the cat studied by means of anterograde axonal transport of labeled amino acids as tracers. Neuroscience 4: 1615–1633Google Scholar
  32. Kawamura K, Hashikawa T (1981) Projections from the pontine nuclei proper and reticular tegmental nucleus onto the cerebellar cortex in the cat. An autoradiographic study. J Comp Neurol 201: 395–413Google Scholar
  33. Kawamura S, Hattori S, Higo S, Matsuyama T (1982) The cerebellar projections to the superior colliculus and pretectum in the cat: an autoradiographic and horseradish peroxidase study. Neuroscience 7: 1673–1689Google Scholar
  34. Keller EL (1979) Colliculoreticular organization in the oculomotor system, In: Granit R, Pompeiano O (eds) Reflex control of posture and movement. Prog Brain Res, Vol 50. Elsevier/North Holland, Amsterdam New York, pp 725–734Google Scholar
  35. Leigh RJ, Zee DS (1983) The saccadic system. In: The neurology of eye movements. Contemporary Neurology Series, Vol 23. FE Davies Co, Philadelphia, pp 39–68Google Scholar
  36. Lin CS, May PJ, Hall WC (1984) Nonintralaminar thalamostriatal projections in the gray squirrel (Sciurus carolinensis) and tree shrew (Tupaia glis). J Comp Neurol 230: 33–46Google Scholar
  37. Lisberger SG (1982) Role of the cerebellum during motor learning in the vestibulo-ocular reflex. Different mechanisms in different species? Trends Neurosci 5: 437–441Google Scholar
  38. Llinás R, Wolfe JW (1977) Functional linkage between the electrical activity in the vermal cerebellar cortex and saccadic eye movements. Exp Brain Res 29: 1–14Google Scholar
  39. Lu SM, Lin C-S, Behan M, Cant NB, Hall WC (1985) Glutamate decarboxylase immunoreactivity in the intermediate grey layer of the superior colliculus in the cat. Neuroscience 16: 123–131Google Scholar
  40. Maekawa K, Takeda T, Kimura M (1981) Neural activity of nucleus reticularis tegmenti pontis — the origin of visual mossy fiber afferents to the cerebellar flocculus of rabbits. Brain Res 210: 17–30Google Scholar
  41. Martin GF, King JS, Dom R (1974) The projections of the deep cerebellar nuclei of the opossum Didelphis marsupialis virginiana. J Hirnforsch 15: 545–573Google Scholar
  42. Matsushita M, Iwahori N (1971) Structural organization of the interpositus and the dentate nuclei. Brain Res 35: 17–36Google Scholar
  43. May PJ, Hall WC (1984) Relationships between the nigrotectal pathway and the cells of origin of the predorsal buncle. J Comp Neurol 226: 357–376Google Scholar
  44. May PJ, Hall WC (1986) Sources of the nigrotectal pathway. Neuroscience 19: 159–180Google Scholar
  45. Mays LE, Sparks DL (1980) Dissociation of visual and saccaderelated responses in superior colliculus neurons. J Neurophysiol 43: 207–232Google Scholar
  46. Mesulam M (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: 106–117PubMedGoogle Scholar
  47. Mohler CW, Wurtz RH (1976) Organization of monkey superior colliculus: intermediate layer cells discharging before eye movements. J Neurophysiol 39: 722–765Google Scholar
  48. Mower G, Gibson A, Glickstein M (1979) Tectopontine pathway in the cat: laminar distribution of cells of origin and visual properties of target cells in dorsolateral pontine nucleus. J Neurophysiol 42: 1–15Google Scholar
  49. Munoz D, Guitton D, Volle M (1984) Tectospinal neuron discharges in the alert headfree cat. Soc Neurosci Abstr 10: 60Google Scholar
  50. Noda H, Suzuki DA (1979) The role of the flocculus of the monkey in saccadic eye movements. J Physiol 294: 317–334Google Scholar
  51. Optican LM, Robinson DA (1980) Cerebellar-dependent adaptive control of primate saccadic system. J Neurophysiol 44: 1058–1076Google Scholar
  52. Rhoades RW, Kuo DC, Polcer JD, Fish SE, Voneida TJ (1982) Indirect visual cortical input to the deep layers of the hamster's superior colliculus via the basal ganglia. J Comp Neurol 208: 239–254Google Scholar
  53. Ritchie L (1976) Effects of cerebellar lesions on saccadic eye movements. J Neurophysiol 39: 1246–1256Google Scholar
  54. Roldán M, Reinoso-Suárez F (1981) Cerebellar projections to the superior colliculus in the cat. J Neurosci 1: 827–834Google Scholar
  55. Ron S, Robinson DA (1973) Eye movements evoked by cerebellar stimulation in the alert monkey. J Neurophysiol 36: 1004–1022Google Scholar
  56. Selhorst JB, Stark L, Ochs AL, Hoyt WF (1976) Disorders in cerebellar ocular motor control. I. Saccadic overshoot dysmetria: an oculographic, control system and clinico-anatomical analysis. Brain 99: 497–508Google Scholar
  57. Sparks DL, Mays LE, Pollack JG (1977) Saccade-related unit activity in the monkey superior colliculus. In: Baker R, Berthoz A (eds) Control of gaze by brainstem neurons. Developments in neuroscience, Vol 1. Elsevier/North Holland Biomedical Press, New York Amsterdam, pp 437–444Google Scholar
  58. Sparks DL, Porter JD (1983) Spatial localization of saccade targets. II. Activity of superior colliculus neurons preceding compensatory saccades. J Neurophysiol 49: 64–74Google Scholar
  59. 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: 699–731Google Scholar
  60. Sugimoto T, Mizuno N, Uchida K (1982) Distribution of cerebellar fiber terminals in the midbrain oculomotor areas: an autoradiographic study in the cat. Brain Res 238: 353–370Google Scholar
  61. Thomas DM, Kaufman RP, Sprague JM, Chambers WW (1956) Experimental studies of the vermal cerebellar projections in the brain. J Anat 90: 371–385Google Scholar
  62. Uchida K, Mizuno N, Sugimoto T, Itoh K, Kudo M (1983) Direct projections from the cerebellar nuclei to the superior colliculus in the rabbit: an HRP study. J Comp Neurol 216: 319–326Google Scholar
  63. Walsh TM, Ebner FF (1973) Distribution of cerebellar and somatic lemniscal projections in the ventral nuclear complex of the Virginia opossum. J Comp Neurol 147: 427–446Google Scholar
  64. Warton S, Jones DG, Ilinsky IA, Kultas-Ilinsky K (1983) Nigral and cerebellar synaptic terminals in the intermediate and deep layers of the cat superior colliculus revealed by lesioning studies. Neuroscience 10: 789–800Google Scholar
  65. Weber JT, Partlow GD, Harting JK (1978) The projection of the superior colliculus upon the inferior olivary complex of the cat: an autoradiographic and horseradish peroxidase study. Brain Res 144: 369–377Google Scholar
  66. Wurtz RH, Albano JR (1980) Visual-motor function of the primate superior colliculus. Ann Rev Neurosci 3: 189–226Google Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • P. J. May
    • 1
  • W. C. Hall
    • 1
  1. 1.Department of AnatomyDuke University Medical CenterDurhamUSA

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