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The Journal of Neuroscience, March 17, 2004, 24(11):2699-2707; doi:10.1523/JNEUROSCI.5176-03.2004

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Cellular/Molecular
Carbonic Anhydrase Isoform VII Acts as a Molecular Switch in the Development of Synchronous Gamma-Frequency Firing of Hippocampal CA1 Pyramidal Cells

Eva Ruusuvuori,¹ Hong Li,^1,2 Kristiina Huttu,¹ J. Matias Palva,¹ Sergei Smirnov,¹ Claudio Rivera,^1,2 Kai Kaila,¹ and Juha Voipio¹

¹Department of Biosciences and ²Institute of Biotechnology, Viikki Biocenter, University of Helsinki, FIN-00014 Helsinki, Finland

Identification of the molecular mechanisms that enable synchronous firing of CA1 pyramidal neurons is central to the understanding of the functional properties of this major hippocampal output pathway. Using microfluorescence measurements of intraneuronal pH, in situ hybridization, as well as intracellular, extracellular, and K⁺-sensitive microelectrode recordings, we show now that the capability for synchronous gamma-frequency (20–80 Hz) firing in response to high-frequency stimulation (HFS) emerges abruptly in the rat hippocampus at approximately postnatal day 12. This was attributable to a steep developmental upregulation of intrapyramidal carbonic anhydrase isoform VII, which acts as a key molecule in the generation of HFS-induced tonic GABAergic excitation. These results point to a crucial role for the developmental expression of intrapyramidal carbonic anhydrase VII activity in shaping integrative functions, long-term plasticity and susceptibility to epileptogenesis.

Key words: carbonic anhydrase; epilepsy; excitatory GABA; gamma oscillations; GDP; hippocampus; potassium; synchrony

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Received Nov 24, 2003; revised January 13, 2004; accepted January 23, 2004.

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