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The Journal of Neuroscience, July 20, 2005, 25(29):6775-6786; doi:10.1523/JNEUROSCI.1135-05.2005

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Cellular/Molecular
Neurogliaform Neurons Form a Novel Inhibitory Network in the Hippocampal CA1 Area

Christopher J. Price,¹ Bruno Cauli,² Endre R. Kovacs,¹ Akos Kulik,³ Bertrand Lambolez,² Ryuichi Shigemoto,^4,5 and Marco Capogna¹

¹Medical Research Council, Anatomical Neuropharmacology Unit, Oxford OX1 3TH, United Kingdom, ²Laboratoire de Neurobiologie et Diversite Cellulaire, Centre National de la Recherche Scientifique, Ecole Superieure de Physique et Chime Industrielles de la ville de Paris, 75005 Paris, France, ³Department of Anatomy and Cell Biology, University of Freiburg, 79104 Freiburg, Germany, ⁴Division of Cerebral Structure, National Institute for Physiological Sciences, Okazaki 444-8787, Japan, and ⁵ Solution Oriented Research for Science and Technology, Japan Science and Technology Corporation, Kawaguchi 332-0012, Japan

We studied neurogliaform neurons in the stratum lacunosum moleculare of the CA1 hippocampal area. These interneurons have short stellate dendrites and an extensive axonal arbor mainly located in the stratum lacunosum moleculare. Single-cell reverse transcription-PCR showed that these neurons were GABAergic and that the majority expressed mRNA for neuropeptide Y. Most neurogliaform neurons tested were immunoreactive for -actinin-2, and many stratum lacunosum moleculare interneurons coexpressed -actinin-2 and neuropeptide Y. Neurogliaform neurons received monosynaptic, DNQX-sensitive excitatory input from the perforant path, and 40 Hz stimulation of this input evoked EPSCs displaying either depression or initial facilitation, followed by depression. Paired recordings performed between neurogliaform neurons showed that 85% of pairs were electrically connected and 70% were also connected via GABAergic synapses. Injection of sine waveforms into neurons during paired recordings resulted in transmission of the waveforms through the electrical synapse. Unitary IPSCs recorded from neurogliaform pairs readily fatigued, had a slow decay, and had a strong depression of the synaptic response at a 5 Hz stimulation frequency that was antagonized by the GABA_B antagonist (2S)-3-[[(1S)-1-(3,4-dichlorophenyl)ethyl]amino-2-hydroxypropyl](phenylmethyl) phosphinic acid (CGP55845. The amplitude of the first IPSC during the 5 Hz stimulation was also increased by CGP55845 suggesting a tonic inhibition of synaptic transmission. A small unitary GABA_B-mediated IPSC could also be detected, providing the first evidence for such a component between GABAergic interneurons. Electron microscopic localization of the GABA_B1 subunit at neurogliaform synapses revealed the protein in both presynaptic and postsynaptic membranes. Our data disclose a novel interneuronal network well suited for modulating the flow of information between the entorhinal cortex and CA1 hippocampus.

Key words: unitary IPSCs; electrical synapses; interneuron; GABA_B; perforant path; short-term plasticity

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Received Dec 14, 2004; revised May 18, 2005; accepted June 6, 2005.

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