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The Journal of Neuroscience, December 5, 2007, 27(49):13499-13512; doi:10.1523/JNEUROSCI.2613-07.2007

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Cellular/Molecular
Synaptic Plasticity and Calcium Signaling in Purkinje Cells of the Central Cerebellar Lobes of Mormyrid Fish

Victor Z. Han,¹ Yueping Zhang,¹ Curtis C. Bell,¹ and Christian Hansel²

¹Neurological Sciences Institute, Oregon Health & Science University, Beaverton, Oregon 97006, and ²Erasmus University Medical Center, Department of Neuroscience, 3000 CA Rotterdam, The Netherlands

Correspondence should be addressed to either of the following: Christian Hansel, Erasmus University Medical Center, Department of Neuroscience, P.O. Box 2040, 3000 CA Rotterdam, The Netherlands, Email: c.hansel{at}erasmusmc.nl; or Victor Z. Han, Neurological Sciences Institute, Oregon Health & Science University, 505 North West 185th Avenue, Beaverton, OR 97006, E-mail: Email: hanv{at}ohsu.edu

Climbing fiber (CF)-evoked calcium transients play a key role in plasticity at parallel fiber (PF) to Purkinje cell synapses in the mammalian cerebellum. Whereas PF activation alone causes long-term potentiation (LTP), coactivation of the heterosynaptic CF input, which evokes large dendritic calcium transients, induces long-term depression (LTD). This unique type of heterosynaptic interaction is a hallmark feature of synaptic plasticity in mammalian Purkinje cells. Purkinje cells in the cerebellum of mormyrid electric fish are characterized by a different architecture of their dendritic trees and by a more pronounced separation of CF and PF synaptic contact sites. We therefore examined the conditions for bidirectional plasticity at PF synapses onto Purkinje cells in the mormyrid cerebellum in vitro. PF stimulation at elevated frequencies induces LTP, whereas LTD results from PF stimulation at enhanced intensities and depends on dendritic calcium influx and metabotropic glutamate receptor type 1 activation. LTD can also be observed after pairing of low intensity PF stimulation with CF stimulation. Using a combination of whole-cell patch-clamp recordings and fluorometric calcium imaging, we characterized calcium transients in Purkinje cell dendrites. CF activation elicits calcium transients not only within the CF input territory (smooth proximal dendrites) but also within the PF input territory (spiny palisade dendrites). Paired PF and CF activation elicits larger calcium transients than stimulation of either input alone. A major source for dendritic calcium signaling is provided by P/Q-type calcium channels. Our data show that despite the spatial separation between the two inputs CF activity facilitates LTD induction at PF synapses.

Key words: cerebellum; Purkinje cell; parallel fiber; climbing fiber; long-term depression; long-term potentiation

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Received June 8, 2007; revised Oct. 26, 2007; accepted Oct. 26, 2007.

Correspondence should be addressed to either of the following: Christian Hansel, Erasmus University Medical Center, Department of Neuroscience, P.O. Box 2040, 3000 CA Rotterdam, The Netherlands, Email: c.hansel{at}erasmusmc.nl; or Victor Z. Han, Neurological Sciences Institute, Oregon Health & Science University, 505 North West 185th Avenue, Beaverton, OR 97006, E-mail: Email: hanv{at}ohsu.edu

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