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.
