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The Journal of Neuroscience, October 15, 2003, 23(28):9320-9327

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Cellular/Molecular
Altered Neuronal Excitability in Cerebellar Granule Cells of Mice Lacking Calretinin

David Gall,¹ Céline Roussel,¹ Isabella Susa,² Egidio D'Angelo,^3,4 Paola Rossi,³ Bertrand Bearzatto,¹ Marie Christine Galas,¹ David Blum,¹ Stéphane Schurmans,⁵ and Serge N. Schiffmann¹

¹Laboratoire de Neurophysiologie (CP601), Faculté deMédecine, Université Libre de Bruxelles, B-1070 Bruxelles, Belgium, ²Optique Nonlinéaire Théorique (CP231), Faculté des Sciences, Université Libre de Bruxelles, B-1050 Bruxelles, Belgium, ³Department of Cellular and Molecular Physiology and Pharmacology, University of Pavia and Instituto Nazionale per la Fisica della Materia, I-27100 Pavia, Italy, ⁴Department of Evolutionary and Functional Biology, University of Parma, 43100 Parma, Italy, and ⁵Institut de Biologie et de Médicine Moléculaires (CP300), Université Libre de Bruxelles, B-6041 Gosselies, Belgium

Calcium-binding proteins such as calretinin are abundantly expressed in distinctive patterns in the CNS, but their physiological function remains poorly understood. Calretinin is expressed in cerebellar granule cells, which provide the major excitatory input to Purkinje cells through parallel fibers. Calretinin-deficient mice exhibit dramatic alterations in motor coordination and Purkinje cell firing recorded in vivo through unknown mechanisms. In the present study, we used patch-clamp recording techniques in acute slice preparation to investigate the effect of a null mutation of the calretinin gene on the intrinsic electroresponsiveness of cerebellar granule cells at a mature developmental stage. Calretinin-deficient granule cells exhibit faster action potentials and generate repetitive spike discharge showing an enhanced frequency increase with injected currents. These alterations disappear when 0.15 mM of the exogenous fast-calcium buffer BAPTA is infused in the cytosol to restore the calcium-buffering capacity. A proposed mathematical model demonstrates that the observed alterations of granule cell excitability can be explained by a decreased cytosolic calcium-buffering capacity resulting from the absence of calretinin. This result suggests that calcium-binding proteins modulate intrinsic neuronal excitability and may therefore play a role in information processing in the CNS.

Key words: calretinin; calcium-binding protein; cerebellar granule cell; excitability; calcium; mathematical model

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Received Feb 5, 2003; revised May 16, 2003; accepted August 15, 2003.

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