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Behavior-dependent specialization of identified hippocampal interneurons

Nature Neuroscience volume 15, pages 1265–1271 (2012)Cite this article

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Abstract

A large variety of GABAergic interneurons control information processing in the hippocampal circuits governing the formation of neuronal representations. Whether distinct hippocampal interneuron types contribute differentially to information processing during behavior is not known. We employed a new technique for recording and labeling interneurons and pyramidal cells in drug-free, freely moving rats. Recorded parvalbumin-expressing basket interneurons innervated somata and proximal pyramidal cell dendrites, whereas nitric oxide synthase– and neuropeptide Y–expressing ivy cells provided synaptic and extrasynaptic dendritic modulation. Basket and ivy cells showed distinct spike-timing dynamics, firing at different rates and times during theta and ripple oscillations. Basket, but not ivy, cells changed their firing rates during movement, sleep and quiet wakefulness, suggesting that basket cells coordinate cell assemblies in a behavioral state–contingent manner, whereas persistently firing ivy cells might control network excitability and homeostasis. Different interneuron types provide GABA to specific subcellular domains at defined times and rates, thereby differentially controlling network activity during behavior.

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Figure 1: Firing patterns of an identified PV-expressing basket cell during different behavioral states.
Figure 2: Firing patterns of an identified ivy cell during different behavioral states.
Figure 3: Molecular expression and firing patterns of a place cell.
Figure 4: Behavioral state segmentation.
Figure 5: Differential firing of PV-expressing basket and ivy cells during distinct behavioral states.
Figure 6: Differential firing of PV-expressing basket and ivy cells during network oscillations.
Figure 7: Relationship between frequency and amplitude of theta oscillations and the firing rate of PV-expressing basket and ivy cells.

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Acknowledgements

The authors thank A. Koroknai for the reconstruction of the dendritic tree of cell D26p, I. Lukacs for the reconstruction of cell TV08k, J. Somogyi for confocal microscopic data acquisition and illustrations, K. Detzner for electron microscopy and immunohistochemistry, R. Hauer and E. Borok for histological processing, T. Sakatani for contributions to microdrive development, B. Micklem for help with the preparation of illustrations, J. O'Neill for help with place cell analysis, Y. Dalezios and G. Dorffner for advice on statistics, and R. Guillery, D. Dupret, M. Capogna, J. Csicsvari and L. Marton for comments on an earlier version of the manuscript. This work was supported in part by grant 242689 of the European Research Council, grant SCIC03 of the Vienna Science and Technology Fund and grant W1205 of the Austrian Science Fund.

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  1. Department of Pharmacology, Medical Research Council Anatomical Neuropharmacology Unit, Oxford University, Oxford, UK

    Damien Lapray, Balint Lasztoczi, Tim James Viney, Linda Katona, Katja Hartwich, Peter Somogyi & Thomas Klausberger

  2. Department of Cognitive Neurobiology, Center for Brain Research, Medical University of Vienna, Vienna, Austria

    Damien Lapray, Balint Lasztoczi, Michael Lagler, Ornella Valenti, Zsolt Borhegyi, Peter Somogyi & Thomas Klausberger

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Lapray, D., Lasztoczi, B., Lagler, M. et al. Behavior-dependent specialization of identified hippocampal interneurons. Nat Neurosci 15, 1265–1271 (2012). https://doi.org/10.1038/nn.3176

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