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Distinct and simultaneously active plasticity mechanisms in mouse hippocampus during different phases of Morris water maze training

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Abstract

Although the Morris water maze (MWM) is the most frequently used protocol to examine hippocampus-dependent learning in mice, not much is known about the spatio-temporal dynamics of underlying plasticity processes. Here, we studied molecular and cellular hippocampal plasticity mechanisms during early and late phases of spatial learning in the MWM. Quantitative in situ hybridization for the immediate early genes zif268 and Homer1a (H1a) revealed phase-dependent differences in their expression between areas CA1 and CA3. During the initial learning phase, CA1 expression levels of the molecular plasticity marker H1a, but not of the activity reporter gene zif268, were related to task proficiency; whereas no learning-specific changes could be detected in CA3. Simultaneously, the ratio of surface-expressed NMDAR subunits NR2A and NR2B was downregulated as measured by acute slice biotinylation assay, while the total number of surface NMDARs was unaltered. When intrinsic ‘somatic’ and synaptic plasticity in the CA1-region of hippocampal slices were examined, we found that early learning promotes intrinsic neuronal plasticity as manifested by a reduction of spike frequency adaptation and postburst afterhyperpolarization. At the synaptic level, however, maintenance of long-term potentiation (LTP) in all learning groups was impaired which is most likely due to ‘intrinsic’ learning-induced LTP which occluded any further electrically induced LTP. Late learning, in contrast, was characterized by re-normalized H1a, NR2A and NR2B expression and neuronal firing, yet a further strengthening of learning-induced LTP. Together, our data support a precisely timed cascade of complex molecular and subcellular transformations occurring from early to late MWM learning.

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Acknowledgments

This work was funded by interdisciplinary research grants from KU Leuven (IDO/06/004 and GOA 12/008). A.L. was supported by a PhD fellowship from the Agency for Innovation by Science and Technology Flanders (IWT-Vlaanderen). J.N. was supported by a PhD fellowship from the Fund for Scientific Research Flanders (FWO-Vlaanderen), and I.G. was supported by a postdoctoral fellowship from FWO-Flanders. We gratefully thank Lieve Geenen for excellent technical assistance. The authors declare no competing financial interest.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Laboratory of Neuroplasticity and Neuroproteomics, KU Leuven, Naamsestraat 59, 3000, Leuven, Belgium

    Annelies Laeremans, Julie Nys, Babs Van de Plas & Lutgarde Arckens

  2. Laboratory of Biological Psychology, KU Leuven, Tiensestraat 102, Box 3714, 3000, Leuven, Belgium

    Victor Sabanov, Tariq Ahmed, Kasper Vinken, Ilse Gantois, Rudi D’Hooge & Detlef Balschun

  3. Laboratory of Movement Control and Neuroplasticity, KU Leuven, Tervuursevest 101, 3001, Heverlee, Belgium

    Daniel G. Woolley

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  1. Annelies Laeremans
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Correspondence to Detlef Balschun.

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Laeremans, A., Sabanov, V., Ahmed, T. et al. Distinct and simultaneously active plasticity mechanisms in mouse hippocampus during different phases of Morris water maze training. Brain Struct Funct 220, 1273–1290 (2015). https://doi.org/10.1007/s00429-014-0722-z

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  • DOI: https://doi.org/10.1007/s00429-014-0722-z

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