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Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area

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  • Christopher J Price, Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Oxford OX1 3TH, United Kingdom, and.
  • ,
  • Bruno Cauli
  • ,
  • Endre R Kovacs
  • ,
  • Akos Kulik
  • ,
  • Bertrand Lambolez
  • ,
  • Ryuichi Shigemoto
  • ,
  • Marco Capogna

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 alpha-actinin-2, and many stratum lacunosum moleculare interneurons coexpressed alpha-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.

Original languageEnglish
JournalThe Journal of neuroscience : the official journal of the Society for Neuroscience
Pages (from-to)6775-86
Number of pages12
Publication statusPublished - 20 Jul 2005

    Research areas

  • Animals, Axons/physiology, Biomarkers, Dendrites/physiology, Electric Stimulation, Entorhinal Cortex/cytology, Hippocampus/cytology, Interneurons/physiology, Nerve Net/cytology, Neural Inhibition/physiology, Neuronal Plasticity/physiology, Organ Culture Techniques, Patch-Clamp Techniques, Perforant Pathway/cytology, Polymerase Chain Reaction, Rats, Rats, Sprague-Dawley, Receptors, GABA-B/genetics

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