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Cerebellar Nuclei and Cerebellar Learning

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Handbook of the Cerebellum and Cerebellar Disorders

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Abstract

The cerebellar nuclei (CN) and the vestibular nucleus are the only recipients of output from the cerebellar cortex and provide the only final output pathway of cerebellar processing. This cortico-nuclear pathway is mediated entirely by GABA inhibition via Purkinje cell (PC) axons, yet conveys important information regarding the fine temporal control of behavior. Therefore, the interesting question arises of how one can control finely tuned CN output spike patterns with inhibition, challenging our understanding of neural coding. Using the technique of dynamic clamp, artificial inhibitory synaptic input patterns can be applied to CN neurons to explore this question. It was found that a population code in which a set of PCs pause at the same time creates an efficient code to precisely trigger individual CN spikes via disinhibition. Strong inhibition can paradoxically also evoke spiking, namely, by a mechanism of postinhibitory rebound, a pronounced property of CN neurons. Strong bursts of PC activity followed by pauses of firing create an ideal stimulus for rebound generation and are elicited by synchronous climbing fiber inputs to cerebellar cortex. Such a stimulus-evoked rebound could trigger specific behavioral responses, though direct evidence for this mechanism is currently lacking. Finally, there are also strong data and modeling results to support a traditional rate coding concepts in the PC to CN connection, which allows for an analog modulation of spike rate in the CN based on equally analog up-and-down modulation of PC spike rates in the opposite direction. These different coding principles are likely to operate in parallel and be important under different behavioral contexts.

The conditioned eyeblink reflex in particular has been extensively studied with respect to learning mechanisms in the CN. Activity in the CN develops an increase just before the eyeblink during learning, and this CN activation depends on plasticity in the excitatory input to CN neurons by mossy fibers. Interestingly, this form of plasticity has been first predicted and then found to be controlled by the activity of inhibitory PC input. The cellular basis for this form of plasticity ultimately depends on a complex set of calcium signaling events during inputs in the required sequence of MF inputs followed by inhibition, followed by repolarization. A similar mechanism is proposed to also underlie the adaptation of vestibulo-ocular gain control coded by the vestibular nuclei. The involvement of similar or different learning mechanisms in the CN in more complex limb movement control remains to be determined, but behavioral and electrophysiological evidence points in the direction that the precise timing of predictive submovement activation in coordinated limb movements may be the predominant function of cerebellar output from the CN in this regard.

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References

  • Abbasi S, Hudson AE, Maran SK, Cao Y, Abbasi A, Heck DH, Jaeger D (2017) Robust transmission of rate coding in the inhibitory Purkinje cell to cerebellar nuclei pathway in awake mice. PLoS Comput Biol 13:e1005578

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aizenman CD, Linden DJ (1999) Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum. J Neurophysiol 82:1697–1709

    Article  CAS  PubMed  Google Scholar 

  • Aizenman CD, Linden DJ (2000) Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat Neurosci 3:109–111

    Article  CAS  PubMed  Google Scholar 

  • Aizenman CD, Manis PB, Linden DJ (1998) Polarity of long-term synaptic gain change is related to postsynaptic spike firing at a cerebellar inhibitory synapse. Neuron 21:827–835

    CAS  PubMed  Google Scholar 

  • Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25–61

    Google Scholar 

  • Alvina K, Walter JT, Kohn A, Ellis-Davies G, Khodakhah K (2008) Questioning the role of rebound firing in the cerebellum. Nat Neurosci 11:1256–1258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Angaut P, Sotelo C (1989) Synaptology of the cerebello-olivary pathway. Double labelling with anterograde axonal tracing and GABA immunocytochemistry in the rat. Brain Res 479:361–365

    Article  CAS  PubMed  Google Scholar 

  • Ankri L, Husson Z, Pietrajtis K, Proville R, Léna C, Yarom Y, Dieudonné S, Uusisaari MY (2015) A novel inhibitory nucleo-cortical circuit controls cerebellar Golgi cell activity. elife 4:e06262

    Google Scholar 

  • Armstrong DM, Edgley SA (1984) Discharges of nucleus interpositus neurones during locomotion in the cat. J Physiol 351:411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Armstrong DM, Rawson JA (1979) Responses of neurones in nucleus interpositus of the cerebellum to cutaneous nerve volleys in the awake cat. J Physiol 289:403–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Armstrong DM, Cogdell B, Harvey R (1975) Effects of afferent volleys from the limbs on the discharge patterns of interpositus neurones in cats anaesthetized with alpha-chloralose. J Physiol 248:489–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beck H, Yaari Y (2008) Plasticity of intrinsic neuronal properties in CNS disorders. Nat Rev Neurosci 9:357–369

    Article  CAS  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 37:10085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bengtsson F, Ekerot CF, Jorntell H (2011) In vivo analysis of inhibitory synaptic inputs and rebounds in deep cerebellar nuclear neurons. PLoS One 6:e18822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berry SD, Hoffmann LC (2011) Hippocampal theta-dependent eyeblink classical conditioning: coordination of a distributed learning system. Neurobiol Learn Mem 95:185–189

    Article  PubMed  Google Scholar 

  • Boele HJ, Koekkoek SKE, De Zeeuw CI (2010) Cerebellar and extracerebellar involvement in mouse eyeblink conditioning: the ACDC model. Front Cell Neurosci 3:19

    Google Scholar 

  • Boyden ES, Katoh A, Raymond JL (2004) Cerebellum-dependent learning: the role of multiple plasticity mechanisms. Annu Rev Neurosci 27:581–609

    Article  CAS  PubMed  Google Scholar 

  • Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263–1268

    Article  CAS  PubMed  Google Scholar 

  • Braitenberg V (1967) Is the cerebellar cortex a biological clock in the millisecond range? Prog Brain Res 25:334–346

    Article  CAS  PubMed  Google Scholar 

  • Broussard DM, Lisberger SG (1992) Vestibular inputs to brain stem neurons that participate in motor learning in the primate vestibuloocular reflex. J Neurophysiol 68:1906–1909

    Article  CAS  PubMed  Google Scholar 

  • Burguiere E, Arabo A, Jarlier F, De Zeeuw CI, Rondi-Reig L (2010) Role of the cerebellar cortex in conditioned goal-directed behavior. J Neurosci 30:13265–13271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campolattaro MM, Kashef A, Lee I, Freeman JH (2011) Neuronal correlates of cross-modal transfer in the cerebellum and pontine nuclei. J Neurosci 31:4051–4062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao Y, Maran SK, Dhamala M, Jaeger D, Heck DH (2012) Behavior-related pauses in simple-spike activity of mouse Purkinje cells are linked to spike rate modulation. J Neurosci 32:8678–8685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan-Palay V (1973) Neuronal plasticity in cerebellar cortex and lateral nucleus. Z Anat Entwicklungsgesch 142:23–35

    Article  CAS  PubMed  Google Scholar 

  • Chan-Palay V (1977) Cerebellar dentate nucleus. Springer, Berlin/Heidelberg

    Book  Google Scholar 

  • Chen S, Hillman DE (1993) Colocalization of neurotransmitters in the deep cerebellar nuclei. J Neurocytol 22:81–91

    Article  CAS  PubMed  Google Scholar 

  • Christian KM, Thompson RF (2003) Neural substrates of Eyeblink conditioning: acquisition and retention. Learn Memory 10:427–455

    Article  Google Scholar 

  • Clopath C, Badura A, De Zeeuw CI, Brunel N (2014) A cerebellar learning model of vestibulo-ocular reflex adaptation in wild-type and mutant mice. J Neurosci 34:7203–7215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooper SE, Martin JH, Ghez C (2000) Effects of inactivation of the anterior interpositus nucleus on the kinematic and dynamic control of multijoint movement. J Neurophysiol 84:1988–2000

    Article  CAS  PubMed  Google Scholar 

  • Crook S, Gleeson P, Howell F, Svitak J, Silver RA (2007) MorphML: level 1 of the NeuroML standards for neuronal morphology data and model specification. Neuroinformatics 5:96–104

    Article  PubMed  PubMed Central  Google Scholar 

  • Crook S, Silver RA, Gleeson P (2009) Describing and exchanging models of neurons and neuronal networks with NeuroML. BMC Neurosci 10:1–2

    Article  Google Scholar 

  • Daoudal G, Debanne D (2003) Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Memory 10:456–465

    Article  Google Scholar 

  • De Schutter E (1995) Cerebellar long-term depression might normalize excitation of Purkinje cells. Trends Neurosci 18:291–295

    Article  PubMed  Google Scholar 

  • De Schutter E, Bower JM (1994) An active membrane model of the cerebellar Purkinje cell I. Simulation of current clamp in slice. J Neurophysiol 71:375–400

    Article  PubMed  Google Scholar 

  • De Schutter E, Steuber V (2009) Patterns and pauses in Purkinje cell simple spike trains: experiments, modeling and theory. Neuroscience 162:816–826

    Article  PubMed  CAS  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 349:428–447

    Article  PubMed  Google Scholar 

  • Desai NS, Rutherford LC, Turrigiano GG (1999) Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat Neurosci 2:515–520

    Article  CAS  PubMed  Google Scholar 

  • Ekerot CF, Jorntell H, Garwicz M (1995) Functional relation between corticonuclear input and movements evoked on microstimulation in cerebellar nucleus interpositus anterior in the cat. Exp Brain Res 106:365–376

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gabbiani F, Midtgaard J, Knöpfel T (1994) Synaptic integration in a model of cerebellar granule cells. JNeurophysiol 72:999–1009

    Article  CAS  Google Scholar 

  • Gao ZY, Proietti-Onori M, Lin ZM, ten Brinke MM, Boele HJ, Potters JW, Ruigrok TJH, Hoebeek FE, De Zeeuw CI (2016) Excitatory cerebellar Nucleocortical circuit provides internal amplification during associative conditioning. Neuron 89:645–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia KS, Steele PM, Mauk MD (1999) Cerebellar cortex lesions prevent acquisition of conditioned eyelid responses. J Neurosci 19:10940–10947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardner EP, Fuchs AF (1975) Single-unit responses to natural vestibular stimuli and eye movements in deep cerebellar nuclei of the alert rhesus monkey. J Neurophysiol 38:627–649

    Article  CAS  PubMed  Google Scholar 

  • Garwicz M, Ekerot CF (1994) Topographical organization of the cerebellar cortical projection to nucleus interpositus anterior in the cat. J Physiol 474:245–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gauck V, Jaeger D (2000) The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition. J Neurosci 20:3006–3016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gauck V, Jaeger D (2003) The contribution of NMDA and AMPA conductances to the control of spiking in neurons of the deep cerebellar nuclei. J Neurosci 23:8109–8118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gleeson P, Steuber V, Silver RA (2007) neuroConstruct: a tool for modeling networks of neurons in 3D space. Neuron 54:219–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gleeson P, Crook S, Cannon RC, Hines ML, Billings GO, Farinella M, Morse TM, Davison AP, Ray S, Bhalla US, Barnes SR, Dimitrova YD, Silver RA (2010) NeuroML: a language for describing data driven models of neurons and networks with a high degree of biological detail. PLoS Comput Biol 6:e1000815

    Article  PubMed  PubMed Central  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Granit R, Phillips CG (1956) Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum of cats. J Physiol (Lond) 133:520–547

    Article  CAS  Google Scholar 

  • Graybiel AM, Nauta HJW, Lasek RJ, Nauta WJH (1973) Cerebello-olivary pathway in cat – experimental study using autoradiographic tracing techniques. Brain Res 58:205–211

    Article  CAS  PubMed  Google Scholar 

  • Grimm RJ, Rushmer DS (1974) The activity of dentate neurons during an arm movement sequence. Brain Res 71:309–326

    Article  CAS  PubMed  Google Scholar 

  • Harvey RJ, Porter R, Rawson JA (1979) Discharges of intracerebellar nuclear cells in monkeys. J Physiol 297:559–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heck DH, De Zeeuw CI, Jaeger D, Khodakhah K, Person AL (2013) The neuronal code(s) of the cerebellum. J Neurosci 33:17603–17609. PMC3818542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heinen SJ, Keller EL (1996) The function of the cerebellar uvula in monkey during optokinetic and pursuit eye movements: single-unit responses and lesion effects. Exp Brain Res 110:1–14

    Article  CAS  PubMed  Google Scholar 

  • Heiney SA, Kim J, Augustine GJ, Medina JF (2014) Precise control of movement kinematics by optogenetic inhibition of Purkinje cell activity. J Neurosci 34:2321–2330

    Article  PubMed  PubMed Central  Google Scholar 

  • Hepp K, Henn V, Jaeger J (1982) Eye movement related neurons in the cerebellar nuclei of the alert monkey. Exp Brain Res 45:253–264

    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 U S A 107:8410–8415. 2889566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffmann LC, Berry SD (2009) Cerebellar theta oscillations are synchronized during hippocampal theta-contingent trace conditioning. Proc Natl Acad Sci 106:21371–21376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holdefer RN, Houk JC, Miller LE (2005) Movement-related discharge in the cerebellar nuclei persists after local injections of GABA(a) antagonists. J Neurophysiol 93:35–43

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa T, Tomatsu S, Tsunoda Y, Lee J, Hoffman DS, Kakei S (2014) Releasing dentate nucleus cells from Purkinje cell inhibition generates output from the Cerebrocerebellum. PLoS One 9:e108774

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ito M (1984) The cerebellum and neural control. Raven Press, New York

    Google Scholar 

  • Ito M (1993) Cerebellar flocculus hypothesis. Nature 363:24–25

    Article  CAS  PubMed  Google Scholar 

  • Ito M (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 81:1143–1195

    Article  CAS  PubMed  Google Scholar 

  • Ito M, Kano M (1982) Long-lasting depression of parallel fiber-Purkinje cell transmission induced by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex. Neurosci Lett 33:253–258

    Article  CAS  PubMed  Google Scholar 

  • Ivry RB (1996) The representation of temporal information in perception and motor control. [review] [51 refs]. Curr Opin Neurobiol 6:851–857

    Article  CAS  PubMed  Google Scholar 

  • Ivry RB, Spencer RMC (2004) The neural representation of time. Curr Opin Neurobiol 14:225–232

    Article  CAS  PubMed  Google Scholar 

  • Jaeger D, Jorntell H, Kawato M (2013) Computation in the cerebellum. Neural Netw Off J Int Neural Netw Soc 47:1–2

    Article  Google Scholar 

  • Jahnsen H (1986a) Extracellular activation and membrane conductances of neurones in the Guinea-pig deep cerebellar nuclei in vitro. J Physiol 372:149–168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jahnsen H (1986b) Electrophysiological characteristics of neurones in the Guinea-pig deep cerebellar nuclei in vitro. J Physiol 372:129–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lisberger SG (1988) The neural basis for learning of simple motor skills. Science 242:728–735

    Article  CAS  PubMed  Google Scholar 

  • Lisberger SG (1994) Neural basis for motor learning in the vestibuloocular reflex of primates. III. Computational and behavioral analysis of the sites of learning. J Neurophysiol 72:974–998

    Article  CAS  PubMed  Google Scholar 

  • Lisberger SG, Pavelko TA, Broussard DM (1994a) Neural basis for motor learning in the vestibuloocular reflex of primates. I. Changes in the responses of brain stem neurons. J Neurophysiol 72:928–953

    Article  CAS  PubMed  Google Scholar 

  • Lisberger SG, Pavelko TA, Bronte-Stewart HM, Stone LS (1994b) Neural basis for motor learning in the vestibuloocular reflex of primates. II. Changes in the responses of horizontal gaze velocity Purkinje cells in the cerebellar flocculus and ventral paraflocculus. J Neurophysiol 72:954–973

    Article  CAS  PubMed  Google Scholar 

  • Llinas R, Muhlethaler M (1988) Electrophysiology of Guinea-pig cerebellar nuclear cells in the in vitro brain stem-cerebellar preparation. J Physiol 404:241–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luque NR, Garrido JA, Naveros F, Carrillo RR, D'Angelo E, Ros E (2016) Distributed cerebellar motor learning: a spike-timing-dependent plasticity model. Front Comput Neurosci 10:17

    Google Scholar 

  • Maex R, De Schutter E (2005) Oscillations in the cerebellar cortex: a prediction of their frequency bands. Prog Brain Res 148:181–188

    Article  PubMed  Google Scholar 

  • Marr D (1969) A theory of cerebellar cortex. J Physiol Lond 202:437–470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsushita M, Iwahori N (1971a) Structural organization of the fastigial nucleus. I. Dendrites and axonal pathways. Brain Res 25:597–610

    Article  CAS  PubMed  Google Scholar 

  • Matsushita M, Iwahori N (1971b) Structural organization of the interpositus and the dentate nuclei. Brain Res 35:17–36

    Article  CAS  PubMed  Google Scholar 

  • Mauk MD (1997) Roles of cerebellar cortex and nuclei in motor learning: contradictions or clues? Neuron 18:343–346

    Article  CAS  PubMed  Google Scholar 

  • McCormick DA, Thompson RF (1984) Neuronal responses of the rabbit cerebellum during acquisition and PERFORMANCE of a classically-conditioned nictitating membrane-eyelid response. J Neurosci 4:2811–2822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCormick DA, Lavond DG, Clark GA, Kettner RE, Rising CE, Thompson RF (1981) The engram found questionable role of the cerebellum in classical-conditioning of nictitating-membrane and eyelid responses. Bull Psychon Soc 18:103–105

    Article  Google Scholar 

  • McCormick DA, Clark GA, Lavond DG, Thompson RF (1982) Initial localization of the memory trace for a basic form of learning. Proc Natl Acad Sci U S A – Biol Sci 79:2731–2735

    Article  CAS  Google Scholar 

  • Medina JF, Mauk MD (1999) Simulations of cerebellar motor learning: computational analysis of plasticity at the mossy fiber to deep nucleus synapse. J Neurosci 19:7140–7151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medina JF, Garcia KS, Nores WL, Taylor NM, Mauk MD (2000) Timing mechanisms in the cerebellum: testing predictions of a large-scale computer simulation. J Neurosci 20:5516–5525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medina JF, Garcia KS, Mauk MD (2001) A mechanism for savings in the cerebellum. J Neurosci 21:4081–4089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milak MS, Bracha V, Bloedel JR (1995) Relationship of simultaneously recorded cerebellar nuclear neuron discharge to the acquisition of a complex, operantly conditioned forelimb movement in cats. Exp Brain Res 105:325–330

    Article  CAS  PubMed  Google Scholar 

  • Milak MS, Shimansky Y, Bracha V, Bloedel JR (1997) Effects of inactivating individual cerebellar nuclei on the Performance and retention of an Operantly conditioned forelimb movement. J Neurophysiol 78:939–959

    Article  CAS  PubMed  Google Scholar 

  • Miles FA, Lisberger SG (1981) Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci 4:273–299

    Article  CAS  PubMed  Google Scholar 

  • Molineux ML, McRory JE, McKay BE, Hamid J, Mehaffey WH, Rehak R, Snutch TP, Zamponi GW, Turner RW (2006) Specific T-type calcium channel isoforms are associated with distinct burst phenotypes in deep cerebellar nuclear neurons. Proc Natl Acad Sci U S A 103:5555–5560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Molineux ML, Mehaffey WH, Tadayonnejad R, Anderson D, Tennent AF, Turner RW (2008) Ionic factors governing rebound burst phenotype in rat deep cerebellar neurons. J Neurophysiol 100:2684–2701

    Article  PubMed  CAS  Google Scholar 

  • Morishita W, Sastry BR (1996) Postsynaptic mechanisms underlying long-term depression of GABAergic transmission in neurons of the deep cerebellar nuclei. J Neurophysiol 76:59–68

    Article  CAS  PubMed  Google Scholar 

  • Nagao S, Honda T, Yamazaki T (2013) Transfer of memory trace of cerebellum-dependent motor learning in human prism adaptation: a model study. Neural Netw 47:72–80

    Article  PubMed  Google Scholar 

  • Najac M, Raman IM (2015) Integration of Purkinje cell inhibition by cerebellar Nucleo-Olivary neurons. J Neurosci 35:544–549

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nelson AB, Krispel CM, Sekirnjak C, du Lac S (2003) Long-lasting increases in intrinsic excitability triggered by inhibition. Neuron 40:609–620

    Article  CAS  PubMed  Google Scholar 

  • Ohtsuka K, Noda H (1991) Saccadic burst neurons in the oculomotor region of the fastigial nucleus of macaque monkeys. J Neurophysiol 65:1422–1434

    Article  CAS  PubMed  Google Scholar 

  • Ohyama T, Nores WL, Mauk MD (2003) Stimulus generalization of conditioned eyelid responses produced without cerebellar cortex: implications for plasticity in the cerebellar nuclei. Learn Memory 10:346–354

    Article  Google Scholar 

  • Ohyama T, Nores WL, Medina JF, Riusech FA, Mauk MD (2006) Learning-induced plasticity in deep cerebellar nucleus. J Neurosci 26:12656–12663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palkovits M, Mezey E, Hamori J, Szentagothai J (1977) Quantitative histological analysis of the cerebellar nuclei in the cat. I. Numerical data on cells and synapses. Exp Brain Res 28:189–209

    CAS  PubMed  Google Scholar 

  • Pedroarena CM, Schwarz C (2003) Efficacy and short-term plasticity at GABAergic synapses between Purkinje and cerebellar nuclei neurons. J Neurophysiol 89:704–715

    Article  CAS  PubMed  Google Scholar 

  • Pellionisz A, Llinás R (1977) A computer model of cerebellar Purkinje cells. Neuroscience 2:37–48

    Article  CAS  PubMed  Google Scholar 

  • Pellionisz A, Llinás R (1979) Brain modeling by tensor network theory and computer simulation. The cerebellum: distributed processor for predictive coordination. Neuroscience 4:323–348

    Article  CAS  PubMed  Google Scholar 

  • Pellionisz A, Szentagothai J (1974) Dynamic single unit simulation of a realistic cerebellar network model. II. Purkinje cell activity within the basic circuit and modified by inhibitory systems. Brain Res 68:19–40

    Article  CAS  PubMed  Google Scholar 

  • Perciavalle V, Apps R, Bracha V, Delgado-Garcia JM, Gibson AR, Leggio M, Carrel AJ, Cerminara N, Coco M, Gruart A, Sanchez-Campusano R (2013) Consensus paper: current views on the role of cerebellar interpositus nucleus in movement control and emotion. Cerebellum 12:738–757

    Article  PubMed  Google Scholar 

  • Perrett SP, Mauk MD (1995) Extinction of conditioned eyelid responses requires the anterior lobe of cerebellar cortex. J Neurosci 15:2074–2080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perrett SP, Ruiz BP, Mauk MD (1993) Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci 13:1708–1718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Person AL, Raman IM (2010) Deactivation of L-type ca current by inhibition controls LTP at excitatory synapses in the cerebellar nuclei. Neuron 66:550–559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Person AL, Raman IM (2012) Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei. Nature 481:502–506

    Article  CAS  Google Scholar 

  • Pugh JR, Raman IM (2006) Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current. Neuron 51:113–123

    Article  CAS  PubMed  Google Scholar 

  • Pugh JR, Raman IM (2008) Mechanisms of potentiation of mossy Fiber EPSCs in the cerebellar nuclei by coincident synaptic excitation and inhibition. J Neurosci 28:10549–10560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Racine RJ, Wilson DA, Gingell R, Sunderland D (1986) Long-term potentiation in the interpositus and vestibular nuclei in the rat. Exp Brain Res 63:158–162

    Article  CAS  PubMed  Google Scholar 

  • Ramachandran R, Lisberger SG (2008) Neural substrate of modified and unmodified pathways for learning in monkey vestibuloocular reflex. J Neurophysiol 100:1868–1878.2576200

    Article  PubMed  PubMed Central  Google Scholar 

  • Raman IM, Gustafson AE, Padgett D (2000) Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J Neurosci 20:9004–9016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond JL, Lisberger SG, Mauk MD (1996) The cerebellum: a neuronal learning machine? Science 272:1126–1131

    Article  CAS  PubMed  Google Scholar 

  • Robinson HPC, Kawai N (1993) Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons. J Neurosci Methods 49:157–165

    Article  CAS  PubMed  Google Scholar 

  • Rowland NC, Jaeger D (2005) Coding of tactile response properties in the rat deep cerebellar nuclei. J Neurophysiol 94:1236–1251

    Article  PubMed  Google Scholar 

  • Rowland NC, Jaeger D (2008) Responses to tactile stimulation in deep cerebellar nucleus neurons result from recurrent activation in multiple pathways. J Neurophysiol 99:704–717

    Article  PubMed  Google Scholar 

  • Sangrey T, Jaeger D (2010) Multiple components of rebound spiking in deep cerebellar nucleus neurons. Eur J Neurosci 32:1646–1657

    Article  PubMed  PubMed Central  Google Scholar 

  • Sato Y, Miura A, Fushiki H, Kawasaki T (1992) Short-term modulation of cerebellar purkinje-cell activity after spontaneous climbing fiber input. J Neurophysiol 68:2051–2062

    Article  CAS  PubMed  Google Scholar 

  • Shaikh AG, Ghasia FF, Dickman JD, Angelaki DE (2005) Properties of cerebellar fastigial neurons during translation, rotation, and eye movements. J Neurophysiol 93:853–863

    Article  PubMed  Google Scholar 

  • Sharp AA, Oneil MB, Abbott LF, Marder E (1993) Dynamic clamp – computer-generated Conductances in real neurons. J Neurophysiol 69:992–995

    Article  CAS  PubMed  Google Scholar 

  • Shin SL, De Schutter E (2006) Dynamic synchronization of Purkinje cell simple spikes. J Neurophysiol 96:3485–3491

    Article  PubMed  Google Scholar 

  • Sjostrom PJ, Rancz EA, Roth A, Hausser M (2008) Dendritic excitability and synaptic plasticity. Physiol Rev 88:769–840

    Article  CAS  PubMed  Google Scholar 

  • Solinas S, Forti L, Cesana E, Mapelli J, De Schutter E, D'Angelo E (2007) Computational reconstruction of pacemaking and intrinsic electroresponsiveness in cerebellar Golgi cells. Front Cell Neurosci 1:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Solinas S, Nieus T, D'Angelo E (2010) A realistic large-scale model of the cerebellum granular layer predicts circuit spatio-temporal filtering properties. Front Cell Neurosci 4:12

    Google Scholar 

  • Steuber V, Schultheiss NW, Silver RA, De Schutter E, Jaeger D (2011) Determinants of synaptic integration and heterogeneity in rebound firing explored with data driven models of deep cerebellar nucleus cells. J Comput Neurosci 30:633–658

    Article  PubMed  Google Scholar 

  • Sudhakar SK, Torben-Nielsen B, De Schutter E (2015) Cerebellar nuclear neurons use time and rate coding to transmit Purkinje neuron pauses. PLoS Comput Biol 11:e1004641. Pmc4668013

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tadayonnejad R, Anderson D, Molineux M, Mehaffey W, Jayasuriya K, Turner R (2010) Rebound discharge in deep cerebellar nuclear neurons in vitro. Cerebellum 9:352–374

    Article  PubMed  PubMed Central  Google Scholar 

  • Telgkamp P, Raman IM (2002) Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei. J Neurosci 22:8447–8457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • ten Brinke MM, Heiney SA, Wang XL, Proietti-Onori M, Boele HJ, Bakermans J, Medina JF, Gao Z, De Zeeuw CI (2017) Dynamic modulation of activity in cerebellar nuclei neurons during pavlovian eyeblink conditioning in mice. elife 6:e28132

    Google Scholar 

  • Teune TM, van der Burg J, de Zeeuw CI, Voogd J, Ruigrok TJ (1998) Single Purkinje cell can innervate multiple classes of projection neurons in the cerebellar nuclei of the rat: a light microscopic and ultrastructural triple-tracer study in the rat. J Comp Neurol 392:164–178

    Article  CAS  PubMed  Google Scholar 

  • Thompson RF, Steinmetz JE (2009) The role of the cerebellum in classical conditioning of discrete behavioral responses. Neuroscience 162:732–755

    Article  CAS  PubMed  Google Scholar 

  • Turecek J, Jackman SL, Regehr WG (2016) Synaptic specializations support frequency-independent Purkinje cell output from the cerebellar cortex. Cell Rep 17:3256–3268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uusisaari M, De Schutter E (2011) The mysterious microcircuitry of the cerebellar nuclei. J Physiol 589:3441–3457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uusisaari MY, Knopfel T (2012) Diversity of neuronal elements and circuitry in the cerebellar nuclei. Cerebellum 11:420–421

    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 97:901–911

    Article  CAS  PubMed  Google Scholar 

  • van Kan PLE, Horn KM, Gibson AR (1994) The importance of hand use to discharge of interpositus neurons of the monkey. J Physiol-Lond 480:171–190

    Article  PubMed  PubMed Central  Google Scholar 

  • Walter JT, Khodakhah K (2009) The advantages of linear information processing for cerebellar computation. Proc Natl Acad Sci U S A 106:4471–4476

    Article  CAS  PubMed  Google Scholar 

  • Wang JJ, Shimansky Y, Bracha V, Bloedel JR (1998) Effects of cerebellar nuclear inactivation on the learning of a complex forelimb movement in cats. J Neurophysiol 79:2447–2459

    Article  CAS  PubMed  Google Scholar 

  • Wetmore DZ, Mukamel EA, Schnitzer MJ (2008) Lock-and-key mechanisms of cerebellar memory recall based on rebound currents. J Neurophysiol 100:2328–2347

    Article  PubMed  Google Scholar 

  • Witter L, Canto CB, Hoogland TM, de Gruijl JR, De Zeeuw CI (2013) Strength and timing of motor responses mediated by rebound firing in the cerebellar nuclei after Purkinje cell activation. Front Neural Circuits 7:133

    Google Scholar 

  • Wulff P, Schonewille M, Renzi M, Viltono L, Sassoe-Pognetto M, Badura A, Gao Z, Hoebeek FE, van Dorp S, Wisden W, Farrant M, De Zeeuw CI (2009) Synaptic inhibition of Purkinje cells mediates consolidation of vestibulo-cerebellar motor learning. Nat Neurosci 12:1042–1049.2718327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Lisberger SG (2014) Role of plasticity at different sites across the time course of cerebellar motor learning. J Neurosci 34:7077–7090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng N, Raman IM (2009) Ca currents activated by spontaneous firing and synaptic disinhibition in neurons of the cerebellar nuclei. J Neurosci 29:9826–9838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Emory University, Atlanta, GA, USA

    Dieter Jaeger

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  1. Dieter Jaeger
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Correspondence to Dieter Jaeger .

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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. Molecular and Integrative Neuroscience Department (MIND), The Scripps Research Institute, La Jolla, California, USA

    Donna L. Gruol

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Jaeger, D. (2019). Cerebellar Nuclei and Cerebellar Learning. 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_47-2

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  • DOI: https://doi.org/10.1007/978-3-319-97911-3_47-2

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  • Print ISBN: 978-3-319-97911-3

  • Online ISBN: 978-3-319-97911-3

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