Complementary roles of cholecystokinin- and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations

被引:335
作者
Klausberger, T
Marton, LF
O'Neill, J
Huck, JHJ
Dalezios, Y
Fuentealba, P
Suen, WY
Papp, E
Kaneko, T
Watanabe, M
Csicsvari, J
Somogyi, P
机构
[1] Univ Oxford, MRC, Anat Neuropharmacol Unit, Oxford OX1 3TH, England
[2] Med Univ, Ctr Brain Res, A-1090 Vienna, Austria
[3] Kyoto Univ, Grad Sch Med, Dept Morphol Brain Sci, Kyoto 6068501, Japan
[4] Hokkaido Univ, Sch Med, Dept Anat, Sapporo, Hokkaido 0603638, Japan
关键词
D O I
10.1523/JNEUROSCI.3269-05.2005
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
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.
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收藏
页码:9782 / 9793
页数:12
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