全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2012 

Sensory Stimulation-Dependent Plasticity in the Cerebellar Cortex of Alert Mice

DOI: 10.1371/journal.pone.0036184

Full-Text   Cite this paper   Add to My Lib

Abstract:

In vitro studies have supported the occurrence of cerebellar long-term depression (LTD), an interaction between the parallel fibers and Purkinje cells (PCs) that requires the combined activation of the parallel and climbing fibers. To demonstrate the existence of LTD in alert animals, we investigated the plasticity of local field potentials (LFPs) evoked by electrical stimulation of the whisker pad. The recorded LFP showed two major negative waves corresponding to trigeminal (broken into the N2 and N3 components) and cortical responses. PC unitary extracellular recording showed that N2 and N3 occurred concurrently with PC evoked simple spikes, followed by an evoked complex spike. Polarity inversion of the N3 component at the PC level and N3 amplitude reduction after electrical stimulation of the parallel fiber volley applied on the surface of the cerebellum 2 ms earlier strongly suggest that N3 was related to the parallel fiber–PC synapse activity. LFP measurements elicited by single whisker pad stimulus were performed before and after trains of electrical stimuli given at a frequency of 8 Hz for 10 min. We demonstrated that during this later situation, the stimulation of the PC by parallel and climbing fibers was reinforced. After 8-Hz stimulation, we observed long-term modifications (lasting at least 30 min) characterized by a specific decrease of the N3 amplitude accompanied by an increase of the N2 and N3 latency peaks. These plastic modifications indicated the existence of cerebellar LTD in alert animals involving both timing and synaptic modulations. These results corroborate the idea that LTD may underlie basic physiological functions related to calcium-dependent synaptic plasticity in the cerebellum.

References

[1]  Ito M, Sakurai M, Tongroach P (1982) Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J Physiol 324: 113–134.
[2]  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.
[3]  Marr D (1969) A theory of cerebellar cortex. J Physiol (Lond) 202: 437–470.
[4]  Albus JS (1971) A theory of cerebellar function. Math Biosci 10: 25–61.
[5]  Ito M (1984) The Cerebellum and Neural Control. New York: Raven.
[6]  De Zeeuw CI, Yeo CH (2005) Time and tide in cerebellar memory formation. Curr Opin Neurobiol 15: 667–674.
[7]  Salin PA, Malenka RC, Nicoll RA (1996) Cyclic AMP mediates a presynaptic form of LTP at cerebellar parallel fiber synapses. Neuron 16: 797–803.
[8]  Lev-Ram V, Wong ST, Storm DR, Tsien RY (2002) A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP. Proc Natl Acad Sci U S A 99: 8389–8393.
[9]  Coesmans M, Weber JT, De Zeeuw CI, Hansel C (2004) Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 44: 691–700.
[10]  Servais L, Hourez R, Bearzatto B, Gall D, Schiffmann SN, et al. (2007) Purkinje cell dysfunction and alteration of long-term synaptic plasticity in fetal alcohol syndrome. Proc Natl Acad Sci U S A 104: 9858–9863.
[11]  Hansel C, Linden DJ (2000) Long-term depression of the cerebellar climbing fiber – Purkinje neuron synapse. Neuron 26: 473–482.
[12]  Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, et al. (1994) Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372: 237–243.
[13]  Crépel F, Krupa M (1988) Activation of protein kinase C induces a long-term depression of glutamate sensitivity of cerebellar Purkinje cells. An in vitro study. Brain Res 458: 397–401.
[14]  Wang YT, Linden DJ (2000) Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron 25: 635–647.
[15]  Hansel C, de Jeu M, Belmeguenai A, Houtman SH, Buitendijk GH, et al. (2006) αCaMKII is essential for cerebellar LTD and motor learning. Neuron 51: 835–843.
[16]  Bidoret C, Ayon A, Barbour B, Casado M (2009) Presynaptic NR2A-containing NMDA receptors implement a high-pass filter synaptic plasticity rule. Pro Natl Acad Sci U S A 106: 14126–14131.
[17]  Piochon C, Levenes C, Ohtsuki G, Hansel C (2010) Purkinje cell NMDA receptors assume a key role in synaptic gain control in the mature cerebellum. J Neurosci 30: 15330–15335.
[18]  Ekerot CF, Kano M (1989) Stimulation parameters including climbing fibre induced long-term depression of parallel fiber synapses. Neurosci Res 6: 264–268.
[19]  Jorntell H, Ekerot CF (2002) Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 34: 797–806.
[20]  Roggeri L, Rivieccio B, Rossi P, D'Angelo E (2008) Tactile stimulation evokes long-term synaptic plasticity in the granular layer of cerebellum. J Neurosci 28: 6354–6359.
[21]  Wang X, Chen G, Gao W, Ebner T (2009) Long-term potentiation of the responses to parallel fiber stimulation in mouse cerebellar cortex in vivo. Neuroscience 162: 713–722.
[22]  Cheron G, Gall D, Servais L, Dan B, Maex R, et al. (2004) Inactivation of calcium-binding protein genes induces 160 Hz oscillations in the cerebellar cortex of alert mice. J Neurosci 24: 434–441.
[23]  Eccles JC, Sasaki K, Strata P (1967) Interpretation of the potential fields generated in the cerebellar cortex by a mossy fibre volley. Exp Brain Res 3: 58–80.
[24]  Chen G, Popa LS, Wang X, Gao W, Barnes J, et al. (2009) Low-frequency oscillations in the cerebellar cortex of the tottering mouse. J Neurophysiol 101: 234–245.
[25]  Cheron G, Sausbier M, Sausbier U, Neuhuber W, Ruth P, et al. (2009) BK channels control cerebellar Purkinje and Golgi cell rhythmicity in vivo. PLoS One 4: e7991.
[26]  Bower JM, Woolston DC (1983) Congruence of spatial organization of tactile projections to granule cell and Purkinje cell layers of cerebellar hemispheres of the albino rat: vertical organization of cerebellar cortex. J Neurophysiol 49: 745–766.
[27]  Morissette J, Bower JM (1996) Contribution of somatosensory cortex to responses in the rat cerebellar granule cell layer following peripheral tactile stimulation. Exp Brain Res 109: 240–250.
[28]  Eccles JC, Llinás RR, Sasaki K (1966) Parallel fibre stimulation and the responses induced thereby in the Purkinje cells of the cerebellum. Exp Brain Res 1: 17–39.
[29]  Llinás RR (1982) General discussion: radial connectivity in the cerebellar cortex: a novel view regarding the functional organization of the molecular layer. In: Palay SL, Chan-Palay V, editors. The Cerebellum: New Vistas New York: Springer Verlag. pp. 189–194.
[30]  Mapelli J, D'Angelo E (2007) The spatial organization of long-term synaptic plasticity at the input stage of cerebellum. J Neurosci 27: 1285–1296.
[31]  Eccles JC, Ito M, Szentágothai J (1967) The Cerebellum as a Neuronal Machine. New York: Springer-Verlag.
[32]  Armstrong DM, Drew T (1980) Responses in the posterior lobe of the rat cerebellum to electrical stimulation of cutaneous afferents to the snout. J Physiol 309: 357–374.
[33]  Sims RE, Hartell NA (2006) Differential susceptibility to synaptic plasticity reveals a functional specialization of ascending axon and parallel fiber synapses to cerebellar Purkinje cells. J Neurosci 26: 5153–5159.
[34]  Isope P, Barbour B (2002) Properties of unitary granule cell – Purkinje cell synapses in adult rat cerebellar slices. J Neurosci 22: 9668–9678.
[35]  Lu H, Esquivel AV, Bower JM (2009) 3D electron microscopic reconstruction of segments of rat cerebellar Purkinje cell dendrites receiving ascending and parallel fiber granule cell synaptic inputs. J Comp Neurol 514: 583–594.
[36]  Daniel H, Levenes C, Crépel F (1998) Cellular mechanisms of cerebellar LTD. Trends Neurosci 21: 401–407.
[37]  Gilbert PF, Thach WT (1977) Purkinje cell activity during motor learning. Brain Res 128: 309–328.
[38]  Ojakangas CL, Ebner TJ (1992) Purkinje cell complex and simple spike changes during a voluntary arm movement learning task in the monkey. J Neurophysiol 68: 2222–2236.
[39]  Medina JF, Lisberger SG (2008) Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. Nat Neurosci 11: 1185–1192.
[40]  Llinás RR, Lang EJ, Welsh JP (1997) The cerebellum, LTD, and memory: alternative views. Learn Mem 3: 445–455.
[41]  Llinás RR, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol 305: 197–213.
[42]  Eilers J, Augustine GJ, Konnerth A (1995) Subthreshold synaptic Ca2+ signalling in fine dendrites and spines of cerebellar Purkinje neurons. Nature 373: 155–158.
[43]  Hartell NA (1996) Strong activation of parallel fibers produces localized calcium transients and a form of LTD that spreads to distant synapses. Neuron 16: 601–610.
[44]  Carvell GE, Simons DJ (1990) Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10: 2638–2648.
[45]  Mégevand P, Troncoso E, Quairiaux C, Muller D, Michel CM, et al. (2009) Long-term plasticity in mouse sensorimotor circuits after rhythmic whisker stimulation. J Neurosci 29: 5326–5335.
[46]  Bosman LW, Koekkoek SK, Shapiro J, Rijken BF, Zandstra F, et al. (2010) Encoding of whisker input by cerebellar Purkinje cells. J Physiol 588: 3757–3783.
[47]  Ebner TJ, Yu QX, Bloedel JR (1983) Increase in Purkinje cell gain associated with naturally activated climbing fiber input. J Neurophysiol 50: 205–219.
[48]  Holtzman T, Rajapaksa T, Mostofi A, Edgley SA (2006) Different responses of rat cerebellar Purkinje cells and Golgi cells evoked by widespread convergent sensory inputs. J Physiol (Lond) 574: 491–507.
[49]  Brunel N, Hakim V, Isope P, Nadal JP, Barbour B (2004) Optimal information storage and the distribution of synaptic weights: perceptron versus Purkinje cell. Neuron 43: 745–757.
[50]  Mittmann W, H?usser M (2007) Linking synaptic plasticity and spike output at excitatory and inhibitory synapses onto cerebellar Purkinje cells. J Neurosci 27: 5559–5570.
[51]  Chen C, Thompson RF (1995) Temporal specificity of long-term depression in parallel fiber-Purkinje synapses in rat cerebellar slice. Learn Mem 2: 185–198.
[52]  Ito M (2002) The molecular organization of cerebellar long-term depression. Nat Rev Neurosci 3: 896–902.
[53]  Poulet JF, Petersen CC (2008) Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454: 881–885.
[54]  Wang SS, Denk W, H?usser M (2000) Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci 3: 1266–1273.
[55]  Steuber V, Mittmann W, Hoebeek FE, Silver RA, De Zeeuw CI (2007) Cerebellar LTD and pattern recognition by Purkinje cells. Neuron 54: 121–136.
[56]  D'Angelo E, De Zeeuw CI (2009) Timing and plasticity in the cerebellum: focus on the granular layer. Trends Neurosci 32: 30–40.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133