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The Journal of Neuroscience, October 19, 2005, 25(42):9782-9793; doi:10.1523/JNEUROSCI.3269-05.2005
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Behavioral/Systems/Cognitive
Complementary Roles of Cholecystokinin- and Parvalbumin-Expressing GABAergic Neurons in Hippocampal Network Oscillations
Thomas Klausberger,1,2 Laszlo F. Marton,1 Joseph O'Neill,1 Jojanneke H. J. Huck,1 Yannis Dalezios,1 Pablo Fuentealba,1 Wai Yee Suen,1 Edit Papp,1 Takeshi Kaneko,3 Masahiko Watanabe,4 Jozsef Csicsvari,1 andPeter Somogyi1 1Medical Research Council Anatomical Neuropharmacology Unit, Oxford University, Oxford OX1 3TH, United Kingdom, 2Center for Brain Research, Medical University, 1090 Vienna, Austria, 3Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, 606-8501 Kyoto, Japan, and 4Department of Anatomy, Hokkaido University School of Medicine, 060-3638 Sapporo, Japan
In the hippocampal CA1 area, a relatively homogenous population of pyramidal cells is accompanied by a diversity of GABAergic interneurons. Previously, we found that parvalbumin-expressing basket, axo-axonic, bistratified, and oriens-lacunosum moleculare cells, innervating different domains of pyramidal cells, have distinct firing patterns during network oscillations in vivo. A second family of interneurons, expressing cholecystokinin but not parvalbumin, is known to target the same domains of pyramidal cells as do the parvalbumin cells. To test the temporal activity of these independent and parallel GABAergic inputs, we recorded the precise spike timing of identified cholecystokinin interneurons during hippocampal network oscillations in anesthetized rats and determined their molecular expression profiles and synaptic targets. The cells were cannabinoid receptor type 1 immunopositive. Contrary to the stereotyped firing of parvalbumin interneurons, cholecystokinin-expressing basket and dendrite-innervating cells discharge, on average, with 1.7 ± 2.0 Hz during high-frequency ripple oscillations in an episode-dependent manner. During theta oscillations, cholecystokinin-expressing interneurons fire with 8.8 ± 3.3 Hz at a characteristic time on the ascending phase of theta waves (155 ± 81°), when place cells start firing in freely moving animals. The firing patterns of some interneurons recorded in drug-free behaving rats were similar to cholecystokinin cells in anesthetized animals. Our results demonstrate that cholecystokinin- and parvalbumin-expressing interneurons make different contributions to network oscillations and play distinct roles in different brain states. We suggest that the specific spike timing of cholecystokinin interneurons and their sensitivity to endocannabinoids might contribute to differentiate subgroups of pyramidal cells forming neuronal assemblies, whereas parvalbumin interneurons contribute to synchronizing the entire network.
Key words: hippocampus; interneurons; cholecystokinin; theta oscillations; ripple oscillations; endocannabinoids; sparse coding
Received April 20, 2005; revised September 8, 2005; accepted September 9, 2005.
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