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The Journal of Neuroscience, September 21, 2005, 25(38):8686-8695; doi:10.1523/JNEUROSCI.2810-05.2005

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Behavioral/Systems/Cognitive
Electrical Coupling between Interneurons with Different Excitable Properties in the Stratum Lacunosum-Moleculare of the Juvenile CA1 Rat Hippocampus

Veronika Zsiros¹ and Gianmaria Maccaferri^1,2

¹Department of Physiology, Feinberg School of Medicine and ²Institute for Neuroscience, Northwestern University, Chicago, Illinois 60611

Electrical coupling among GABAergic interneurons is believed to play an essential role in shaping synchronized brain network activity related to cognition and behavior. We have studied the rules governing the electrical coupling between hippocampal interneurons located in stratum lacunosum-moleculare of the CA1 hippocampus. The most frequently recorded interneuron subtype had short multipolar dendrites and a dense local axonal arborization, typical of neurogliaform cells. Electrical excitability in this class of interneurons was heterogeneous. Although injection of small current steps evoked late spiking, larger steps triggered different types of firing patterns. Trains of action potentials ranged from clearly adapting to highly irregular, with clustered or mostly regular spikes. Electrotonic and action potentials could be propagated to the coupled cells; the coupling coefficient for electrotonic signals was 0.035, which compared with 0.005 for action potentials. Electrical coupling was reversibly blocked by application of carbenoxolone. Multiple simultaneous recordings indicated that interneurons with similar and different firing patterns were electrically coupled. This visual impression was quantitatively confirmed by principal component analysis applied to variables related to membrane excitability. In fact, the probability of finding electrically coupled neurons in our sample was not dependent on the excitable properties of the cells tested and was 0.34. The presence of diffuse electrical coupling among hippocampal interneurons of stratum lacunosum-moleculare with different excitability is a novel finding with important implications. For example, the promiscuity of electrical connections may endow inhibitory networks with a large degree of flexibility and regulate the computational power of the hippocampus during different synchronized states.

Key words: interneuron; GABA; gap junction; connexin; pannexin; hippocampus

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Received March 16, 2005; revised August 2, 2005; accepted August 10, 2005.

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