Skip to main content
SpringerLink
Log in

Cerebellar Influences on Descending Spinal Motor Systems

  • Living reference work entry
  • First Online:
Handbook of the Cerebellum and Cerebellar Disorders

  • 133 Accesses

Abstract

The cerebellar nuclei, and to some extent the vestibular nuclei, mediate the ultimate result of cerebellar processing to the rest of the brain. Cerebellar output is directed to the diencephalon and to a score of brainstem regions. This chapter reviews the cerebellar nuclear projections to the brainstem areas that give rise to descending connections that can influence motor programming at spinal cord level, i.e., the reticulospinal, vestibulospinal, rubrospinal, tectospinal, and interstitiospinal pathways. In addition, cerebellar projections to other areas will be briefly considered. Although cerebellar output is structured by the modular internal organization of cerebellar circuitry and related olivocerebellar connections, it is concluded that the modular output, i.e., output of individual cerebellar nuclei or parts thereof, still reaches many areas in the brainstem and diencephalon. In addition, multiple modules may converge their outputs indirectly to the same muscles. This suggests that multiple modules may each take part in different aspects of control of the same muscle or muscle group. Conversely, individual modules, due to the distributed nature of their outputs, may simultaneously affect several descending motor systems with the same ensuing goal. Tools for detailed anatomical and physiological studies are now available and are expected to enhance our knowledge on the effects of the cerebellum on descending motor pathways.

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

Access this chapter

Log in via an institution

Institutional subscriptions

Abbreviations

12:

Hypoglossal nucleus

3V:

3rd ventricle

4/5 Cb:

Cerebellar lobule 4/5

4V:

4th ventricle

7:

Facial nucleus

AIN:

Anterior interposed nucleus

Amb:

Ambiguus nucleus

AP:

Anterior pretectal nucleus

Aq:

Aquaduct

BIN:

Basal interstitial nucleus

BPN:

Basilar pontine nuclei

Cbl:

Cerebellum

CG:

Central gray

CN:

Cerebellar nuclei

cp:

Cerebral peduncle

D:

Nucleus of Darkschewitsch

DLH:

Dorsolateral hump

Ecu:

External cuneate nucleus

FF:

Fields of Forel

fr:

Retroflex fascicle

Gi:

Gigantocellular reticular nucleus

IC:

Inferior colliculus

ICG:

Interstitial cell groups

icp:

Inferior cerebellar peduncle

INC:

Interstitial nucleus of Cajal

IO:

Inferior olive

IV:

Fourth ventricle

LCN:

Lateral cerebellar nucleus

LG:

Lateral geniculate nucleus

LRN:

Lateral reticular nucleus

LV:

Lateral vestibular nucleus

MCN:

Medial cerebellar nucleus

mcp:

Middle cerebellar peduncle

Md:

Medullary reticular nucleus

MG:

Medial geniculate nucleus

ml:

Medial lemniscus

mlf:

Medial longitudinal fascicle

Mo5:

Motor trigeminal nucleus

MV:

Medial vestibular nucleus

n7:

Facial nerve

NRTP:

Nucleus reticularis tegmenti pontis

PAG:

Periaqueductal gray

PCRt:

Parvicellular reticular formation

PF:

Parafascicular thalamic nucleus

Pfl:

Paraflocculus

PIN:

Posterior interposed nucleus

PnC:

Caudal pontine reticular formation

PnO:

Oral pontine reticular formation

py:

Pyramidal tract

RN:

Red nucleus

RNm:

Magnocellular red nucleus

RNp:

Parvicellular red nucleus

SC:

Superior colliculus

scp:

Superior cerebellar peduncle

Sim:

Simple lobule

SN:

Substantia nigra

SO:

Superior olive

Sp5:

Spinal trigeminal nucleus

SpV:

Spinal vestibular nucleus

SuV:

Superior vestibular nucleus

VTh:

Ventral group thalamic nuclei

ZI:

Zona incerta

References

  • Al-Izki S, Kirkwood PA, Lemon RN, Enriquez Denton M (2008) Electrophysiological actions of the rubrospinal tract in the anaesthetised rat. Exp Neurol 212(1):118–131

    PubMed  Google Scholar 

  • Allen GI, Tsukahara N (1974) Cerebrocerebellar communication systems. Physiol Rev 54(4): 957–1006

    CAS  PubMed  Google Scholar 

  • Angaut P, Cicirata F (1990) Dentate control pathways of cortical motor activity. Anatomical and physiological studies in rat: comparative considerations. Arch Ital Biol 128(2–4):315–330

    CAS  PubMed  Google Scholar 

  • Ankri L, Husson Z, Pietrajtis K, Proville R, Lena C, Yarom Y, Dieudonne S, Uusisaari MY (2015) A novel inhibitory nucleo-cortical circuit controls cerebellar Golgi cell activity. Elife 4. https://doi.org/10.7554/eLife.06262

  • Apps R, Garwicz M (2005) Anatomical and physiological foundations of cerebellar information processing. Nat Rev 6(4):297–311

    CAS  Google Scholar 

  • Apps R, Hawkes R (2009) Cerebellar cortical organization: a one-map hypothesis. Nat Rev 10(9):670–681

    CAS  Google Scholar 

  • Apps R, Strata P (2015) Neuronal circuits for fear and anxiety – the missing link. Nat Rev 16(10):642. https://doi.org/10.1038/nrn4028

    Article  CAS  Google Scholar 

  • Arber S (2017) Organization and function of neuronal circuits controlling movement. EMBO Mol Med 9(3):281–284. https://doi.org/10.15252/emmm.201607226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arshavsky YI, Gelfand IM, Orlovsky GN (1986) Cerebellum and rhythmical movements. Studies of brain function, vol 13. Springer, Berlin/Heidelberg

    Google Scholar 

  • Arshavsky YI, Orlovsky GN, Perret C (1988) Activity of rubrospinal neurons during locomotion and scratching in the cat. Behav Brain Res 28(1–2):193–199

    CAS  PubMed  Google Scholar 

  • Asanuma C, Thach WT, Jones EG (1983) Brainstem and spinal projections of the deep cerebellar nuclei in the monkey, with observations on the brainstem projections of the dorsal column nuclei. Brain Res 286(3):299–322

    CAS  PubMed  Google Scholar 

  • Aumann TD, Rawson JA, Finkelstein DI, Horne MK (1994) Projections from the lateral and interposed cerebellar nuclei to the thalamus of the rat: a light and electron microscopic study using single and double anterograde labelling. J Comp Neurol 349(2):165–181. https://doi.org/10.1002/cne.903490202

    Article  CAS  PubMed  Google Scholar 

  • Bagnall MW, Zingg B, Sakatos A, Moghadam SH, Zeilhofer HU, du Lac S (2009) Glycinergic projection neurons of the cerebellum. J Neurosci 29(32):10104–10110

    Google Scholar 

  • Balaban CD, Porter JD (1998) Neuroanatomic substrates for vestibulo-autonomic interactions. J Vestib Res 8(1):7–16

    CAS  PubMed  Google Scholar 

  • Balaban CD, Schuerger RJ, Porter JD (2000) Zonal organization of flocculo-vestibular connections in rats. Neuroscience 99(4):669–682

    CAS  PubMed  Google Scholar 

  • Bankoul S, Neuhuber WL (1992) A direct projection from the medial vestibular nucleus to the cervical spinal dorsal horn of the rat, as demonstrated by anterograde and retrograde tracing. Anat Embryol 185(1):77–85

    CAS  Google Scholar 

  • Bantli H, Bloedel JR (1975) Monosynaptic activation of a direct reticulo-spinal pathway by the dentate nucleus. Pflugers Arch 357(3–4):237–242

    CAS  PubMed  Google Scholar 

  • Batini C, Buisseret-Delmas C, Compoint C, Daniel H (1989) The GABAergic neurones of the cerebellar nuclei in the rat: projections to the cerebellar cortex. Neurosci Lett 99:251–256

    CAS  PubMed  Google Scholar 

  • Batini C, Compoint C, Buisseret-Delmas C, Daniel H, Guegan M (1992) Cerebellar nuclei and the nucleocortical projections in the rat: retrograde tracing coupled to GABA and glutamate immunohistochemistry. J Comp Neurol 315:74–84

    CAS  PubMed  Google Scholar 

  • Batton RR, Jayaraman D, Ruggiero D, Carpenter MB (1977) Fastigial afferent projections in the monkey: an autoradiographic study. J Comp Neurol 174:281–306

    PubMed  Google Scholar 

  • Beitzel CS, Houck BD, Lewis SM, Person AL (2017) Rubrocerebellar feedback loop isolates the interposed nucleus as an independent processor of corollary discharge information in mice. J Neurosci 37(42):10085–10096. https://doi.org/10.1523/JNEUROSCI.1093-17.2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bentivoglio M, Kuypers HGJM (1982) Divergent axon collaterals from rat cerebellar nuclei to diencephalon, mesencephalon, medulla oblongata and cervical cord. Exp Brain Res 46:339–356

    CAS  PubMed  Google Scholar 

  • Bentivoglio M, Molinari M (1985) Crossed divergent axon collaterals from cerebellar nuclei to thalamus and lateral medulla oblongata in the rat. Brain Res 362:180–184

    Google Scholar 

  • Bernard JF (1987) Topographical organization of olivocerebellar and corticonuclear connections in the rat – an WGA-HRP study: I. Lobules IX, X, and the flocculus. J Comp Neurol 263(2): 241–258

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bianchi R, Gioia M (1995) Fine structure of the interstitial nucleus of Cajal of the cat. J Anat 187(Pt 1):141–150

    PubMed  PubMed Central  Google Scholar 

  • Boesten AJP, Voogd J (1985) Hypertrophy of neurons in the inferior olive after cerebellar ablations in the cat. Neurosci Lett 61:49–54

    CAS  PubMed  Google Scholar 

  • Bradley DJ, Ghelarducci B, Spyer KM (1991) The role of the posterior cerebellar vermis in cardiovascular control. Neurosci Res 12(1):45–56. https://doi.org/10.1016/0168-0102(91)90099-K

    Article  CAS  PubMed  Google Scholar 

  • Brodal A (1974) Anatomy of the vestibular nuclei and their connections. In: Kornhuber HH (ed) Handbook of sensory physiology, vol VI, I: Vestibular system. Springer, New York, pp 239–352

    Google Scholar 

  • Buisseret-Delmas C, Angaut P (1988) The cerebellar nucleo-cortical projections in the rat. A retrograde labeling study using horseradish peroxidase combined to a lectin. Neurosci Lett 84:255–260

    CAS  PubMed  Google Scholar 

  • Buisseret-Delmas C, Yatim N, Buisseret P, Angaut P (1993) The X zone and CX subzone of the cerebellum in the rat. Neurosci Res 16:195–207

    CAS  PubMed  Google Scholar 

  • Buisseret-Delmas C, Angaut P, Compoint C, Diagne M, Buisseret P (1998) Brainstem efferents from the interface between the nucleus medialis and the nucleus interpositus in the rat. J Comp Neurol 402:264–275

    CAS  PubMed  Google Scholar 

  • Buttner-Ennever JA (2006) The extraocular motor nuclei: organization and functional neuroanatomy. Prog Brain Res 151:95–125

    CAS  PubMed  Google Scholar 

  • Capelli P, Pivetta C, Soledad Esposito M, Arber S (2017) Locomotor speed control circuits in the caudal brainstem. Nature 551(7680):373–377. https://doi.org/10.1038/nature24064

    Article  CAS  PubMed  Google Scholar 

  • Carlton SM, Leichnetz GR, Mayer DJ (1982) Projections from the nucleus parafascicularis prerubralis to medullary raphe nuclei and inferior olive in the rat: a horseradish peroxidase and autoradiography study. Neurosci Lett 30:191–197

    CAS  PubMed  Google Scholar 

  • Cerminara NL, Apps R (2010) Behavioural significance of cerebellar modules. Cerebellum. https://doi.org/10.1007/s12311-010-0209-2

  • Cerminara NL, Aoki H, Loft M, Sugihara I, Apps R (2013) Structural basis of cerebellar microcircuits in the rat. J Neurosci 33(42):16427–16442. https://doi.org/10.1523/JNEUROSCI.0861-13.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan-Palay V (1977) Cerebellar dentate nucleus: organization, cytology and transmitters. Springer, Berlin

    Google Scholar 

  • Cicirata F, Angaut P, Serapide MF, Panto MR, Nicotra G (1992) Multiple representation in the nucleus lateralis of the cerebellum: an electrophysiologic study in the rat. Exp Brain Res 89(2):352–362

    CAS  PubMed  Google Scholar 

  • Collewijn H (1975) Oculomotor areas in the rabbits midbrain and pretectum. J Neurobiol 6(1):3–22

    CAS  PubMed  Google Scholar 

  • Conde F (1988) Cerebellar projections to the red nucleus of the cat. Behav Brain Res 28(1–2):65–68

    CAS  PubMed  Google Scholar 

  • Daniel H, Billard JM, Angaut P, Batini C (1987) The interposito-rubrospinal system. Anatomical tracing of a motor control pathway in the rat. Neurosci Res 5(2):87–112

    CAS  PubMed  Google Scholar 

  • De Zeeuw CI, Ruigrok TJH (1994) Olivary projecting neurons in the nucleus of Darkschewitsch in the cat receive excitatory monosynaptic input from the cerebellar nuclei. Brain Res 653: 345–350

    PubMed  Google Scholar 

  • De Zeeuw CI, Holstege JC, Ruigrok TJH, Voogd J (1989) Ultrastructural study of the GABAergic, cerebellar and mesodiencephalic innervation of the cat medial accessory olive: anterograde tracing combined with immunocytochemistry. J Comp Neurol 284:12–35

    PubMed  Google Scholar 

  • De Zeeuw CI, Wylie DR, DiGiorgi PL, Simpson JI (1994) Projections of individual Purkinje cells of identified zones in the flocculus to the vestibular and cerebellar nuclei in the rabbit. J Comp Neurol 349(3):428–447

    PubMed  Google Scholar 

  • Delfini C, Diagne M, Angaut P, Buisseret P, Buisseret-Delmas C (2000) Dentatovestibular projections in the rat. Exp Brain Res 135(3):285–292

    CAS  PubMed  Google Scholar 

  • Ding SL, Royall JJ, Sunkin SM, Ng L, Facer BA, Lesnar P, Guillozet-Bongaarts A, McMurray B, Szafer A, Dolbeare TA, Stevens A, Tirrell L, Benner T, Caldejon S, Dalley RA, Dee N, Lau C, Nyhus J, Reding M, Riley ZL, Sandman D, Shen E, van der Kouwe A, Varjabedian A, Write M, Zollei L, Dang C, Knowles JA, Koch C, Phillips JW, Sestan N, Wohnoutka P, Zielke HR, Hohmann JG, Jones AR, Bernard A, Hawrylycz MJ, Hof PR, Fischl B, Lein ES (2016) Comprehensive cellular-resolution atlas of the adult human brain. J Comp Neurol 524(16): 3127–3481. https://doi.org/10.1002/cne.24080

    Article  PubMed  PubMed Central  Google Scholar 

  • Enderle JD (2002) Neural control of saccades. Prog Brain Res 140:21–49

    PubMed  Google Scholar 

  • Esposito MS, Capelli P, Arber S (2014) Brainstem nucleus MdV mediates skilled forelimb motor tasks. Nature 508(7496):351–356. https://doi.org/10.1038/nature13023

    Article  CAS  PubMed  Google Scholar 

  • Fields H (2004) State-dependent opioid control of pain. Nat Rev 5(7):565–575

    CAS  Google Scholar 

  • Fredette BJ, Mugnaini E (1991) The GABAergic cerebello-olivary projection in the rat. Anat Embryol 184:225–243

    CAS  Google Scholar 

  • Fujikado T, Noda H (1987) Saccadic eye movements evoked by microstimulation of lobule VII of the cerebellar vermis of macaque monkeys. J Physiol 394:573–594

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fukushima K (1991) The interstitial nucleus of Cajal in the midbrain reticular formation and vertical eye movement. Neurosci Res 10(3):159–187

    CAS  PubMed  Google Scholar 

  • Fukushima K, van der Hoeff-van Halen R, Peterson BW (1978) Direct excitation of neck motoneurons by interstitiospinal fibers. Exp Brain Res 33(3–4):565–581

    Google Scholar 

  • Fukushima-Kudo J, Fukushima K, Tashiro K (1987) Rigidity and dorsiflexion of the neck in progressive supranuclear palsy and the interstitial nucleus of Cajal. J Neurol Neurosurg Psychiatry 50(9):1197–1203

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao Z, Proietti-Onori M, Lin Z, Ten Brinke MM, Boele HJ, Potters JW, Ruigrok TJ, Hoebeek FE, De Zeeuw CI (2016) Excitatory cerebellar nucleocortical circuit provides internal amplification during associative conditioning. Neuron 89(3):645–657. S0896-6273(16)00009-X

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gautier JC, Blackwood W (1961) Enlargement of the inferior olivary nucleus in association with lesions of the central tegmental tract or dentate nucleus. Brain 84:341–363

    CAS  PubMed  Google Scholar 

  • Gayer NS, Faull RL (1988) Connections of the paraflocculus of the cerebellum with the superior colliculus in the rat brain. Brain Res 449(1–2):253–270

    CAS  PubMed  Google Scholar 

  • Glickstein M, Gerrits N, Kralj-Hans I, Mercier B, Stein J, Voogd J (1994) Visual pontocerebellar projections in the macaque. J Comp Neurol 349(1):51–72

    CAS  PubMed  Google Scholar 

  • Gonzalo-Ruiz A, Leichnetz GR (1987) Collateralization of cerebellar efferent projections to the paraoculomotor region, superior colliculus, and medial pontine reticular formation in the rat: a fluorescent double labeling study. Exp Brain Res 68:365–378

    CAS  PubMed  Google Scholar 

  • Gonzalo-Ruiz A, Leichnetz GR, Smith DJ (1988) Origin of cerebellar projections to the region of the oculomotor complex, medial pontine reticular formation, and superior colliculus in New World monkeys: a retrograde horseradish peroxidase study. J Comp Neurol 268(4):508–526

    CAS  PubMed  Google Scholar 

  • Goodman DC, Hallett RE, Welch RB (1963) Patterns of localization in the cerebellar corticonuclear projections of albino rat. J Comp Neurol 121:51–67

    CAS  PubMed  Google Scholar 

  • Graf W, Gerrits N, Yatim-Dhiba N, Ugolini G (2002) Mapping the oculomotor system: the power of transneuronal labelling with rabies virus. Eur J Neurosci 15(9):1557–1562

    PubMed  Google Scholar 

  • Guillain GC, Mollaret P, Bertrand IG (1933) Sur la lesion responsable du syndrome myoclonique de tronc cerebral. Rev Neurol (Paris) 3:666–673

    Google Scholar 

  • Haines DE, Dietrichs E, Mihailoff GA, McDonald EF (1997) The cerebellar-hypothalamic axis: basic circuits and clinical observations. Int Rev Neurobiol 41:83–107

    CAS  PubMed  Google Scholar 

  • Hannig S, Jurgens U (2006) Projections of the ventrolateral pontine vocalization area in the squirrel monkey. Exp Brain Res 169(1):92–105

    CAS  PubMed  Google Scholar 

  • Harting JK (1977) Descending pathways from the superior collicullus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). J Comp Neurol 173(3):583–612

    CAS  PubMed  Google Scholar 

  • Hicks TP, Onodera S (2012) The mammalian red nucleus and its role in motor systems, including the emergence of bipedalism and language. Prog Neurobiol 96(2):165–175. https://doi.org/10.1016/j.pneurobio.2011.12.002

    Article  PubMed  Google Scholar 

  • Highstein SM, Holstein GR (2006) The anatomy of the vestibular nuclei. Prog Brain Res 151: 157–203

    CAS  PubMed  Google Scholar 

  • 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):1–12

    CAS  PubMed  Google Scholar 

  • Hoebeek FE, Witter L, Ruigrok TJ, De Zeeuw CI (2010) Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei. Proc Natl Acad Sci USA 107:8410

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holstege G, Cowie RJ (1989) Projections from the rostral mesencephalic reticular formation to the spinal cord. An HRP and autoradiographical tracing study in the cat. Exp Brain Res 75(2):265–279

    CAS  PubMed  Google Scholar 

  • Holstege G, Kuypers HG (1982) The anatomy of brain stem pathways to the spinal cord in cat. A labeled amino acid tracing study. Prog Brain Res 57:145–175

    CAS  PubMed  Google Scholar 

  • Holstege JC, Kuypers HG (1987) Brainstem projections to spinal motoneurons: an update. Neuroscience 23(3):809–821

    CAS  PubMed  Google Scholar 

  • Horn AK, Buttner-Ennever JA (1998) Premotor neurons for vertical eye movements in the rostral mesencephalon of monkey and human: histologic identification by parvalbumin immunostaining. J Comp Neurol 392(4):413–427

    CAS  PubMed  Google Scholar 

  • Horn KM, Pong M, Batni SR, Levy SM, Gibson AR (2002) Functional specialization within the cat red nucleus. J Neurophysiol 87(1):469–477

    CAS  PubMed  Google Scholar 

  • Horn KM, Pong M, Gibson AR (2010) Functional relations of cerebellar modules of the cat. J Neurosci 30(28):9411–9423. https://doi.org/10.1523/JNEUROSCI.0440-10.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houck BD, Person AL (2015) Cerebellar premotor output neurons collateralize to innervate the cerebellar cortex. J Comp Neurol 523(15):2254–2271. https://doi.org/10.1002/cne.23787

    Article  PubMed  PubMed Central  Google Scholar 

  • Huisman AM, Kuypers HG, Conde F, Keizer K (1983) Collaterals of rubrospinal neurons to the cerebellum in rat. A retrograde fluorescent double labeling study. Brain Res 264(2):181–196

    CAS  PubMed  Google Scholar 

  • Ilg UJ, Thier P (2008) The neural basis of smooth pursuit eye movements in the rhesus monkey brain. Brain Cogn 68(3):229–240

    PubMed  Google Scholar 

  • Ito M, Yoshida M (1966) The origin of cerebellar-induced inhibition of Deiters’ neurones. I. Monosynaptic initiation of the inhibitory postsynaptic potentials. Exp Brain Res 2:330–349

    CAS  PubMed  Google Scholar 

  • Kakei S, Muto N, Shinoda Y (1994) Innervation of multiple neck motor nuclei by single reticulospinal tract axons receiving tectal input in the upper cervical spinal cord. Neurosci Lett 172(1–2):85–88

    CAS  PubMed  Google Scholar 

  • Kasumacic N, Lambert FM, Coulon P, Bras H, Vinay L, Perreault MC, Glover JC (2015) Segmental organization of vestibulospinal inputs to spinal interneurons mediating crossed activation of thoracolumbar motoneurons in the neonatal mouse. J Neurosci 35(21):8158–8169. https://doi.org/10.1523/JNEUROSCI.5188-14.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(7):1673–1689

    CAS  PubMed  Google Scholar 

  • Kennedy PR (1990) Corticospinal, rubrospinal and rubro-olivary projections: a unifying hypothesis. Trends Neurosci 13:474–479

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Koutsikou S, Crook JJ, Earl EV, Leith JL, Watson TC, Lumb BM, Apps R (2014) Neural substrates underlying fear-evoked freezing: the periaqueductal grey-cerebellar link. J Physiol 592(10): 2197–2213. https://doi.org/10.1113/jphysiol.2013.268714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kralj-Hans I, Baizer JS, Swales C, Glickstein M (2007) Independent roles for the dorsal paraflocculus and vermal lobule VII of the cerebellum in visuomotor coordination. Exp Brain Res 177(2):209–222

    PubMed  Google Scholar 

  • Kuchler M, Fouad K, Weinmann O, Schwab ME, Raineteau O (2002) Red nucleus projections to distinct motor neuron pools in the rat spinal cord. J Comp Neurol 448(4):349–359

    PubMed  Google Scholar 

  • Kurimoto Y, Kawaguchi S, Murata M (1995) Cerebellotectal projection in the rat: anterograde and retrograde WGA-HRP study of individual cerebellar nuclei. Neurosci Res 22(1):57–71

    CAS  PubMed  Google Scholar 

  • Kuypers HGJM (1981) Anatomy of the descending pathways. In: Brookhart JM, Mountcastle VB, VBrooks VB, Geiger SR (eds) Handbook of physiology. Volume II, Motor control Part 1. American Physiological Society, Bethesda, pp 597–666

    Google Scholar 

  • Kuypers HGJM (1985) The anatomical and functional organization of the output of the motor system. In: Swash E (ed) Science basis of clinical neurology. Churchill Livingstone, Edinburgh, pp 1–17

    Google Scholar 

  • Lambert FM, Bras H, Cardoit L, Vinay L, Coulon P, Glover JC (2016) Early postnatal maturation in vestibulospinal pathways involved in neck and forelimb motor control. Dev Neurobiol 76(10):1061–1077. https://doi.org/10.1002/dneu.22375

    Article  CAS  PubMed  Google Scholar 

  • Langer TP (1985) Basal interstitial nucleus of the cerebellum: cerebellar nucleus related to the flocculus. J Comp Neurol 235:38–47

    CAS  PubMed  Google Scholar 

  • Lee HS, Kosinski RJ, Mihailoff GA (1989) Collateral branches of cerebellopontine axons reach the thalamus, superior colliculus or inferior olive: a double-fluorescence and combined fluorescence-horseradish peroxidase study in the rat. Neuroscience 28:725–735

    CAS  PubMed  Google Scholar 

  • Lu X, Miyachi S, Ito Y, Nambu A, Takada M (2007) Topographic distribution of output neurons in cerebellar nuclei and cortex to somatotopic map of primary motor cortex. Eur J Neurosci 25(8):2374–2382

    PubMed  Google Scholar 

  • Luo P, Moritani M, Dessem D (2001) Jaw-muscle spindle afferent pathways to the trigeminal motor nucleus in the rat. J Comp Neurol 435(3):341–353

    CAS  PubMed  Google Scholar 

  • May PJ, Hall WC (1986) The cerebellotectal pathway in the grey squirrel. Exp Brain Res 65(1):200–212

    CAS  PubMed  Google Scholar 

  • May PJ, Hartwich-Young R, Nelson J, Sparks DL, Porter JD (1990) Cerebellotectal pathways in the macaque: implications for collicular generation of saccades. Neuroscience 36(2):305–324

    CAS  PubMed  Google Scholar 

  • Mehler WR (1967) Double descending pathways originating from the superior cerebellar peduncle: an example of neural species differences. Anat Rec 157:374

    Google Scholar 

  • Meredith MA, Miller LK, Ramoa AS, Clemo HR, Behan M (2001) Organization of the neurons of origin of the descending pathways from the ferret superior colliculus. Neurosci Res 40(4):301–313

    CAS  PubMed  Google Scholar 

  • Miller LE, Gibson AR (2009) Red nucleus. In: Squire LR (ed) Encyclopedia of neuroscience, vol 8. Elsevier, Amsterdam, pp 55–62

    Google Scholar 

  • Mock M, Butovas S, Schwarz C (2006) Functional unity of the ponto-cerebellum: evidence that intrapontine communication is mediated by a reciprocal loop with the cerebellar nuclei. J Neurophysiol 95(6):3414–3425. https://doi.org/10.1152/jn.01060.2005

    Article  PubMed  Google Scholar 

  • Morcuende S, Delgado-Garcia JM, Ugolini G (2002) Neuronal premotor networks involved in eyelid responses: retrograde transneuronal tracing with rabies virus from the orbicularis oculi muscle in the rat. J Neurosci 22(20):8808–8818

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muir GD, Whishaw IQ (2000) Red nucleus lesions impair overground locomotion in rats: a kinetic analysis. Eur J Neurosci 12(3):1113–1122

    CAS  PubMed  Google Scholar 

  • Murray EA, Coulter JD (1982) Organization of tectospinal neurons in the cat and rat superior colliculus. Brain Res 243(2):201–214

    CAS  PubMed  Google Scholar 

  • Muto N, Kakei S, Shinoda Y (1996) Morphology of single axons of tectospinal neurons in the upper cervical spinal cord. J Comp Neurol 372(1):9–26

    CAS  PubMed  Google Scholar 

  • Najac M, Raman IM (2015) Integration of Purkinje cell inhibition by cerebellar nucleo-olivary neurons. J Neurosci 35(2):544–549. https://doi.org/10.1523/JNEUROSCI.3583-14.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura H, Wu R, Watanabe K, Onozuka M, Itoh K (2006) Projections of glutamate decarboxylase positive and negative cerebellar neurons to the pretectum in the cat. Neurosci Lett 403(1–2):30–34

    CAS  PubMed  Google Scholar 

  • Newman DB (1985a) Distinguishing rat brainstem reticulospinal nuclei by their neuronal morphology. I. Medullary nuclei. J Hirnforsch 26:187–226

    CAS  PubMed  Google Scholar 

  • Newman DB (1985b) Distinguishing rat brainstem reticulospinal nuclei by their neuronal morphology. II. Pontine and mesencephalic nuclei. J Hirnforsch 26:385–418

    CAS  PubMed  Google Scholar 

  • Noda H (1991) Cerebellar control of saccadic eye movements: its neural mechanisms and pathways. Jpn J Physiol 41(3):351–368

    CAS  PubMed  Google Scholar 

  • Noda H, Fujikado T (1987) Topography of the oculomotor area of the cerebellar vermis in macaques as determined by microstimulation. J Neurophysiol 58(2):359–378

    CAS  PubMed  Google Scholar 

  • Noda H, Sugita S, Ikeda Y (1990) Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. J Comp Neurol 302(2):330–348

    CAS  PubMed  Google Scholar 

  • Nudo RJ, Masterton RB (1989) Descending pathways to the spinal cord: II. Quantitative study of the tectospinal tract in 23 mammals. J Comp Neurol 286(1):96–119

    CAS  PubMed  Google Scholar 

  • Nyberg-Hansen R (1964a) The location and termination of tectospinal fibers in the cat. Exp Neurol 9:212–227

    CAS  PubMed  Google Scholar 

  • Nyberg-Hansen R (1964b) Origin and termination of fibers from the vestibular nuclei descending in the medial longitudinal fasciculus. An experimental study with silver impregnation methods in the cat. J Comp Neurol 122:355–367

    CAS  PubMed  Google Scholar 

  • Nyberg-Hansen R (1965) Sites and mode of termination of reticulo-spinal fibers in the cat. An experimental study with silver impregnation methods. J Comp Neurol 124:71–99

    CAS  PubMed  Google Scholar 

  • Olivier E, Kitama T, Grantyn A (1994) Anatomical evidence for ipsilateral collicular projections to the spinal cord in the cat. Exp Brain Res 100(1):160–164

    CAS  PubMed  Google Scholar 

  • Olivier E, Grantyn A, Kitama T, Berthoz A (1995) Post-spike facilitation of neck EMG by cat tectoreticulospinal neurones during orienting movements. J Physiol 482(Pt 2):455–466

    CAS  PubMed  PubMed Central  Google Scholar 

  • Onodera S, Hicks TP (1999) Evolution of the motor system: why the elephant’s trunk works like a human’s hand. Neuroscientist 5(4):217–226

    Google Scholar 

  • Onodera S, Hicks TP (2009) A comparative neuroanatomical study of the red nucleus of the cat, macaque and human. PLoS One 4(8):e6623

    PubMed  PubMed Central  Google Scholar 

  • Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, 4th edn. Academic, San Diego

    Google Scholar 

  • Paxinos G, Huang X-F, Toga AW (2000) The rhesus monkey in stereotaxic coordinates. Academic, San Diego

    Google Scholar 

  • Peterson BW, Maunz RA, Pitts NG, Mackel RG (1975) Patterns of projection and branching of reticulospinal neurons. Exp Brain Res 23(4):333–351

    CAS  PubMed  Google Scholar 

  • Pijpers A, Voogd J, Ruigrok TJ (2005) Topography of olivo-cortico-nuclear modules in the intermediate cerebellum of the rat. J Comp Neurol 492(2):193–213

    PubMed  Google Scholar 

  • Pijpers A, Apps R, Pardoe J, Voogd J, Ruigrok TJ (2006) Precise spatial relationships between mossy fibers and climbing fibers in rat cerebellar cortical zones. J Neurosci 26(46): 12067–12080

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pijpers A, Winkelman BH, Bronsing R, Ruigrok TJ (2008) Selective impairment of the cerebellar C1 module involved in rat hind limb control reduces step-dependent modulation of cutaneous reflexes. J Neurosci 28(9):2179–2189

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pong M, Horn KM, Gibson AR (2008) Pathways for control of face and neck musculature by the basal ganglia and cerebellum. Brain Res Rev 58(2):249–264

    PubMed  Google Scholar 

  • Prevosto V, Graf W, Ugolini G (2010) Cerebellar inputs to intraparietal cortex areas LIP and MIP: functional frameworks for adaptive control of eye movements, reaching, and arm/eye/head movement coordination. Cereb Cortex 20(1):214–228

    PubMed  Google Scholar 

  • Provini L, Marcotti W, Morara S, Rosina A (1998) Somatotopic nucleocortical projections to the multiple somatosensory cerebellar maps. Neuroscience 83:1085–1104

    CAS  PubMed  Google Scholar 

  • Rajakumar N, Hrycyshyn AW, Flumerfelt BA (1992) Afferent organization of the lateral reticular nucleus in the rat: an anterograde tracing study. Anat Embryol 185(1):25–37

    CAS  Google Scholar 

  • Ralston DD (1994) Cerebellar terminations in the red nucleus of Macaca fascicularis: an electron-microscopic study utilizing the anterograde transport of WGA:HRP. Somatosens Mot Res 11(2):101–107

    CAS  PubMed  Google Scholar 

  • Robinson FR, Cohen JL, May J, Sestokas AK, Glickstein M (1984) Cerebellar targets of visual pontine cells in the cat. J Comp Neurol 223(4):471–482

    CAS  PubMed  Google Scholar 

  • Robinson FR, Houk JC, Gibson AR (1987) Limb specific connections of the cat magnocellular red nucleus. J Comp Neurol 257(4):553–577

    CAS  PubMed  Google Scholar 

  • Rose PK, Abrahams VC (1978) Tectospinal and tectoreticular cells: their distribution and afferent connections. Can J Physiol Pharmacol 56(4):650–658

    CAS  PubMed  Google Scholar 

  • Rubertone JA, Haroian AJ, Vincent SL, Mehler WR (1990) The rat parvocellular reticular formation: I. Afferents from the cerebellar nuclei. Neurosci Lett 119(1):79–82

    CAS  PubMed  Google Scholar 

  • Ruigrok TJ (1997) Cerebellar nuclei: the olivary connection. Prog Brain Res 114:167–192

    CAS  PubMed  Google Scholar 

  • Ruigrok TJ (2003) Collateralization of climbing and mossy fibers projecting to the nodulus and flocculus of the rat cerebellum. J Comp Neurol 466(2):278–298

    PubMed  Google Scholar 

  • Ruigrok TJH (2004) Precerebellar nuclei and red nucleus. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier Academic, San Diego, pp 167–204

    Google Scholar 

  • Ruigrok TJ (2011) Ins and outs of cerebellar modules. Cerebellum 10(3):464–474. https://doi.org/10.1007/s12311-010-0164-y

    Article  PubMed  Google Scholar 

  • Ruigrok TJ, Teune TM (2014) Collateralization of cerebellar output to functionally distinct brainstem areas. A retrograde, non-fluorescent tracing study in the rat. Front Syst Neurosci 8:23. https://doi.org/10.3389/fnsys.2014.00023

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruigrok TJH, Voogd J (1990) Cerebellar nucleo-olivary projections in rat. An anterograde tracing study with Phaseolus vulgaris-leucoagglutinin (PHA-L). J Comp Neurol 298:315–333

    CAS  PubMed  Google Scholar 

  • Ruigrok TJH, Voogd J (1995) Cerebellar influence on olivary excitability in the cat. Eur J Neurosci 7:679–693

    CAS  PubMed  Google Scholar 

  • Ruigrok TJ, Voogd J (2000) Organization of projections from the inferior olive to the cerebellar nuclei in the rat. J Comp Neurol 426(2):209–228

    CAS  PubMed  Google Scholar 

  • Ruigrok TJH, de Zeeuw CI, Voogd J (1990) Hypertrophy of inferior olivary neurons: a degenerative, regenerative or plasticity phenomenon. Eur J Morphol 28:224–239

    CAS  PubMed  Google Scholar 

  • Ruigrok TJH, Osse R-J, Voogd J (1992) Organization of inferior olivary projections to the flocculus and ventral paraflocculus of the rat cerebellum. J Comp Neurol 316:129–150

    CAS  PubMed  Google Scholar 

  • Ruigrok TJH, Teune TM, van der Burg J, Sabel-Goedknegt H (1995) A retrograde double labeling technique for light microscopy. A combination of axonal transport of cholera toxin B-subunit and a gold-lectin conjugate. J Neurosci Methods 61:127–138

    CAS  PubMed  Google Scholar 

  • Ruigrok TJ, Pijpers A, Goedknegt-Sabel E, Coulon P (2008) Multiple cerebellar zones are involved in the control of individual muscles: a retrograde transneuronal tracing study with rabies virus in the rat. Eur J Neurosci 28(1):181–200. https://doi.org/10.1111/j.1460-9568.2008.06294.x

    Article  PubMed  Google Scholar 

  • Ruigrok TJH, Sillitoe RV, Voogd J (2015) Cerebellum and cerebellar connections. In: Paxinos G (ed) The rat nervous system, 4th edn. Elsevier, Amsterdam, pp 133–205

    Google Scholar 

  • Rutherford JG, Anderson WA, Gwyn DG (1984) A reevaluation of midbrain and diencephalic projections to the inferior olive in rat with particular reference to the rubro-olivary pathway. J Comp Neurol 229:285–300

    CAS  PubMed  Google Scholar 

  • Saper CB (2004) Central autonomic system. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier Academic, San Diego, pp 761–796

    Google Scholar 

  • Schonewille M, Luo C, Ruigrok TJ, Voogd J, Schmolesky MT, Rutteman M, Hoebeek FE, De Jeu MT, De Zeeuw CI (2006) Zonal organization of the mouse flocculus: physiology, input, and output. J Comp Neurol 497(4):670–682

    PubMed  Google Scholar 

  • Sekirnjak C, Vissel B, Bollinger J, Faulstich M, du Lac S (2003) Purkinje cell synapses target physiologically unique brainstem neurons. J Neurosci 23(15):6392–6398

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shaikh AG, Hong S, Liao K, Tian J, Solomon D, Zee DS, Leigh RJ, Optican LM (2010) Oculopalatal tremor explained by a model of inferior olivary hypertrophy and cerebellar plasticity. Brain 133(Pt 3):923–940

    PubMed  PubMed Central  Google Scholar 

  • Shapovalov AI (1972) Extrapyramidal monosynaptic and disynaptic control of mammalian alpha-motoneurons. Brain Res 40(1):105–115

    CAS  PubMed  Google Scholar 

  • Shapovalov AI, Gurevitch NR (1970) Monosynaptic and disynaptic reticulospinal actions on lumbar motoneurons of the rat. Brain Res 21(2):249–263

    CAS  PubMed  Google Scholar 

  • Shinoda Y, Ghez C, Arnold A (1977) Spinal branching of rubrospinal axons in the cat. Exp Brain Res 30(2–3):203–218

    CAS  PubMed  Google Scholar 

  • Shinoda Y, Futami T, Mitoma H, Yokota J (1988) Morphology of single neurones in the cerebello-rubrospinal system. Behav Brain Res 28:59–64

    CAS  PubMed  Google Scholar 

  • Shinoda Y, Sugiuchi Y, Izawa Y, Hata Y (2006) Long descending motor tract axons and their control of neck and axial muscles. Prog Brain Res 151:527–563

    PubMed  Google Scholar 

  • Shokunbi MT, Hrycyshyn AW, Flumerfelt BA (1986) A horseradish peroxidase study of the rubral and cortical afferents to the lateral reticular nucleus in the rat. J Comp Neurol 248(3):441–454. https://doi.org/10.1002/cne.902480312

    Article  CAS  PubMed  Google Scholar 

  • 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(4):699–731

    CAS  PubMed  Google Scholar 

  • Sugihara I, Shinoda Y (2004) Molecular, topographic, and functional organization of the cerebellar cortex: a study with combined aldolase C and olivocerebellar labeling. J Neurosci 24(40): 8771–8785

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sugihara I, Shinoda Y (2007) Molecular, topographic, and functional organization of the cerebellar nuclei: analysis by three-dimensional mapping of the olivonuclear projection and aldolase C labeling. J Neurosci 27(36):9696–9710

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sugihara I, Ebata S, Shinoda Y (2004) Functional compartmentalization in the flocculus and the ventral dentate and dorsal group y nuclei: an analysis of single olivocerebellar axonal morphology. J Comp Neurol 470(2):113–133

    PubMed  Google Scholar 

  • Sugimoto T, Mizuno N, Uchida K (1982) Distribution of cerebellar fiber terminals in the midbrain visuomotor areas: an autoradiographic study in the cat. Brain Res 238(2):353–370

    CAS  PubMed  Google Scholar 

  • Takagi M, Zee DS, Tamargo RJ (1998) Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. J Neurophysiol 80(4):1911–1931

    CAS  PubMed  Google Scholar 

  • Tan J, Epema AH, Voogd J (1995) Zonal organization of the flocculovestibular nucleus projection in the rabbit: a combined axonal tracing and acetylcholinesterase histochemical study. J Comp Neurol 356(1):51–71

    CAS  PubMed  Google Scholar 

  • Tang Y, Rampin O, Giuliano F, Ugolini G (1999) Spinal and brain circuits to motoneurons of the bulbospongiosus muscle: retrograde transneuronal tracing with rabies virus. J Comp Neurol 414(2):167–192

    CAS  PubMed  Google Scholar 

  • ten Donkelaar HJ (1988) Evolution of the red nucleus and rubrospinal tract. Behav Brain Res 28(1–2):9–20

    PubMed  Google Scholar 

  • Teune TM, Van der Burg J, Ruigrok TJH (1995) Cerebellar projections to the red nucleus and inferior olive originate from separate populations of neurons in the rat. A non-fluorescent double labeling study. Brain Res 673:313–319

    CAS  PubMed  Google Scholar 

  • Teune TM, van der Burg J, van der Moer J, Voogd J, Ruigrok TJ (2000) Topography of cerebellar nuclear projections to the brain stem in the rat. Prog Brain Res 124:141–172

    CAS  PubMed  Google Scholar 

  • Thach WT, Bastian AJ (2004) Role of the cerebellum in the control and adaptation of gait in health and disease. Prog Brain Res 143:353–366

    PubMed  Google Scholar 

  • Thier P, Dicke PW, Haas R, Thielert CD, Catz N (2002) The role of the oculomotor vermis in the control of saccadic eye movements. Ann N Y Acad Sci 978:50–62

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Tolbert DL, Bantli H, Hames EG, Ebner TJ, McMullen TA, Bloedel JR (1980) A demonstration of the dentato-reticulospinal projection in the cat. Neuroscience 5(8):1479–1488

    CAS  PubMed  Google Scholar 

  • Torvik A, Brodal A (1957) The origin of reticulospinal fibers in the cat; an experimental study. Anat Rec 128(1):113–137

    CAS  PubMed  Google Scholar 

  • Travers JB, DiNardo LA, Karimnamazi H (2000) Medullary reticular formation activity during ingestion and rejection in the awake rat. Exp Brain Res 130(1):78–92

    CAS  PubMed  Google Scholar 

  • Tsukahara N, Bando T, Murakami F, Oda Y (1983) Properties of cerebello-precerebellar reverberating circuits. Brain Res 274:249–259

    CAS  PubMed  Google Scholar 

  • 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(3):319–326

    CAS  PubMed  Google Scholar 

  • Uusisaari M, Knopfel T (2010) GlyT2+ neurons in the lateral cerebellar nucleus. Cerebellum 9(1):42–55. https://doi.org/10.1007/s12311-009-0137-1

    Article  PubMed  Google Scholar 

  • Uusisaari M, Obata K, Knopfel T (2007) Morphological and electrophysiological properties of GABAergic and non-GABAergic cells in the deep cerebellar nuclei. J Neurophysiol 97(1): 901–911

    CAS  PubMed  Google Scholar 

  • van der Steen J, Simpson JI, Tan J (1994) Functional and anatomic organization of three-dimensional eye movements in rabbit cerebellar flocculus. J Neurophysiol 72(31–46):31–46

    PubMed  Google Scholar 

  • Voogd J (1964) The cerebellum of the cat: structure and fiber connections. Van Gorcum, Assen

    Google Scholar 

  • Voogd J (2004) Cerebellum. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier Academic, San Diego, pp 205–242

    Google Scholar 

  • Voogd J (2011) Cerebellar zones: a personal history. Cerebellum 10(3):334–350. https://doi.org/10.1007/s12311-010-0221-6

    Article  PubMed  Google Scholar 

  • Voogd J (2016) Deiters’ nucleus. Its role in cerebellar ideogenesis: the Ferdinando Rossi memorial lecture. Cerebellum 15(1):54–66. https://doi.org/10.1007/s12311-015-0681-9

    Article  PubMed  Google Scholar 

  • Voogd J, Barmack NH (2006) Oculomotor cerebellum. Prog Brain Res 151:231–268

    PubMed  Google Scholar 

  • Voogd J, Glickstein M (1998) The anatomy of the cerebellum. Trends Neurosci 2:305–371

    Google Scholar 

  • Voogd J, Ruigrok TJ (2004) The organization of the corticonuclear and olivocerebellar climbing fiber projections to the rat cerebellar vermis: the congruence of projection zones and the zebrin pattern. J Neurocytol 33(1):5–21

    PubMed  Google Scholar 

  • Voogd J, Ruigrok TJH (2012) Cerebellum and precerebellar nuclei. In: Mai JK, Paxinos G (eds) The human nervous system, 3rd edn. Elsevier, Amsterdam, pp 471–545

    Google Scholar 

  • Voogd J, Wylie DR (2004) Functional and anatomical organization of floccular zones: a preserved feature in vertebrates. J Comp Neurol 470(2):107–112. https://doi.org/10.1002/cne.11022

    Article  PubMed  Google Scholar 

  • Voogd J, Gerrits NM, Ruigrok TJH (1996) Organization of the vestibulocerebellum. Ann N Y Acad Sci 781:553–579

    CAS  PubMed  Google Scholar 

  • 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(3):789–800

    CAS  PubMed  Google Scholar 

  • Whishaw IQ, Gorny B, Sarna J (1998) Paw and limb use in skilled and spontaneous reaching after pyramidal tract, red nucleus and combined lesions in the rat: behavioral and anatomical dissociations. Behav Brain Res 93(1–2):167–183

    CAS  PubMed  Google Scholar 

  • Wylie DR, De Zeeuw CI, DiGiorgi PL, Simpson JI (1994) Projections of individual Purkinje cells of identified zones in the ventral nodulus to the vestibular and cerebellar nuclei in the rabbit. J Comp Neurol 349(3):448–463

    CAS  PubMed  Google Scholar 

  • Wylie DR, Gutierrez-Ibanez C, Corfield JR, Craciun I, Graham DJ, Hurd PL (2017) Inferior olivary projection to the zebrin II stripes in lobule IXcd of the pigeon flocculus: a retrograde tracing study. J Comp Neurol 525(14):3158–3173. https://doi.org/10.1002/cne.24270

    Article  CAS  PubMed  Google Scholar 

  • Ye C, Bogovic JA, Ying SH, Prince JL (2013) Segmentation of the complete superior cerebellar peduncles using a multi-object geometric deformable model. Proc IEEE Int Symp Biomed Imaging 2013:49–52. https://doi.org/10.1109/ISBI.2013.6556409

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu JN, Wang JJ (2008) The cerebellum in feeding control: possible function and mechanism. Cell Mol Neurobiol 28(4):469–478. https://doi.org/10.1007/s10571-007-9236-z

    Article  PubMed  Google Scholar 

  • Zuk A, Rutherford JG, Gwyn DG (1983) Projections from the interstitial nucleus of Cajal to the inferior olive and to the spinal cord in cat: a retrograde fluorescent double-labeling study. Neurosci Lett 38(2):95–101

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Dutch Ministry of Health, Welfare and Sports (T.R.).

Author information

Authors and Affiliations

  1. Department of Neuroscience, Erasmus Medical Center Rotterdam, Rotterdam, The Netherlands

    Tom J. H. Ruigrok

Authors
  1. Tom J. H. Ruigrok
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tom J. H. Ruigrok .

Editor information

Editors and Affiliations

  1. Bruxelles, Belgium

    Mario Manto

  2. Scripps Research Institute Dept. Neuropharmacology, La Jolla, CA, USA

    Donna Gruol

  3. Dept. Neurology, Harvard Medical School Massachusetts General Hospital, Boston, MA, USA

    Jeremy Schmahmann

  4. Gunma University Dept. Integrative Physiology, Maebashi, Gunma, Japan

    Noriyuki Koibuchi

  5. Dept Pathology & Immunology & Neuro, Baylor College of Medicine Dept Pathology & Immunology & Neuro, Houston, TX, USA

    Roy Sillitoe

Section Editor information

  1. Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA

    Jeremy D. Schmahmann

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this entry

Check for updates. Verify currency and authenticity via CrossMark

Cite this entry

Ruigrok, T.J.H. (2020). Cerebellar Influences on Descending Spinal Motor Systems. In: Manto, M., Gruol, D., Schmahmann, J., Koibuchi, N., Sillitoe, R. (eds) Handbook of the Cerebellum and Cerebellar Disorders. Springer, Cham. https://doi.org/10.1007/978-3-319-97911-3_23-2

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-97911-3_23-2

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-97911-3

  • Online ISBN: 978-3-319-97911-3

  • eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences

Publish with us

Policies and ethics

Search

Navigation