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The Journal of Neuroscience, May 11, 2005, 25(19):4813-4822; doi:10.1523/JNEUROSCI.0410-05.2005

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Cellular/Molecular
Intracellular Calcium Regulation by Burst Discharge Determines Bidirectional Long-Term Synaptic Plasticity at the Cerebellum Input Stage

David Gall,^1,2,4 Francesca Prestori,^1,2 Elisabetta Sola,^1,2 Anna D'Errico,¹ Celine Roussel,⁴ Lia Forti,^1,2 Paola Rossi,^1,2 and Egidio D'Angelo^1,2,3

¹Department of Cellular-Molecular Physiological and Pharmacological Sciences, University of Pavia, I-27100 Pavia, Italy, ²National Institute for the Physics of Matter, I-16152 Genova, Italy, ³Department of Functional and Evolutionary Biology, University of Parma, I-34100 Parma, Italy, and ⁴Laboratoire de Neurophysiologie (CP601), Faculte de Medecine, Universite de Bruxelles, B-1070 Bruxelles, Belgium

Variations in intracellular calcium concentration ([Ca²⁺]_i) provide a critical signal for synaptic plasticity. In accordance with Hebb's postulate (Hebb, 1949), an increase in postsynaptic [Ca²⁺]_i can induce bidirectional changes in synaptic strength depending on activation of specific biochemical pathways (Bienenstock et al., 1982; Lisman, 1989; Stanton and Sejnowski, 1989). Despite its strategic location for signal processing, spatiotemporal dynamics of [Ca²⁺]_i changes and their relationship with synaptic plasticity at the cerebellar mossy fiber (mf)-granule cell (GrC) relay were unknown. In this paper, we report the plasticity/[Ca²⁺]_i relationship for GrCs, which are typically activated by mf bursts (Chadderton et al., 2004). Mf bursts caused a remarkable [Ca²⁺]_i increase in GrC dendritic terminals through the activation of NMDA receptors, metabotropic glutamate receptors (probably acting through IP₃-sensitive stores), voltage-dependent calcium channels, and Ca²⁺-induced Ca²⁺ release. Although [Ca²⁺]_i increased with the duration of mf bursts, long-term depression was found with a small [Ca²⁺]_i increase (bursts <250 ms), and long-term potentiation (LTP) was found with a large [Ca²⁺]_i increase (bursts >250 ms). LTP and [Ca²⁺]_i saturated for bursts >500 ms and with theta-burst stimulation. Thus, bursting enabled a Ca²⁺-dependent bidirectional Bienenstock-Cooper-Munro-like learning mechanism providing the cellular basis for effective learning of burst patterns at the input stage of the cerebellum.

Key words: calcium; LTP; LTD; synaptic plasticity; cerebellum; granule cells

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Received Jan 31, 2005; revised April 5, 2005; accepted April 5, 2005.

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