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The Journal of Neuroscience, October 1, 2008, 28(40):10017-10022; doi:10.1523/JNEUROSCI.2052-08.2008
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Brief Communications
Rhythmically Active Enkephalin-Expressing GABAergic Cells in the CA1 Area of the Hippocampus Project to the Subiculum and Preferentially Innervate Interneurons
Pablo Fuentealba,1 Ryohei Tomioka,1,2 Yannis Dalezios,1,3,4 László F. Márton,1,5 Michele Studer,6 Kathleen Rockland,2 Thomas Klausberger,1 andPeter Somogyi1 1Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Oxford OX1 3TH, United Kingdom, 2Laboratory of Cortical Organization and Systematics, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan, 3Department of Basic Sciences, Faculty of Medicine, University of Crete, GR-71003 Heraklion, Greece, 4Institute of Applied and Computational Mathematics, Foundation of Research and Technology–Hellas, GR-71110 Heraklion, Greece, 5Neural Systems Research Group, Sapientia-Hungarian University of Transylvania, Targu Mures, Romania, and 6Telethon Institute of Genetics and Medicine, 80131 Naples, Italy
Correspondence should be addressed to either Pablo Fuentealba or Peter Somogyi, Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford OX1 3TH, UK. Email: pablo.fuentealba{at}pharm.ox.ac.uk or Email: peter.somogyi{at}pharm.ox.ac.uk
Enkephalins (ENKs) are endogenous opioids that regulate synaptic excitability of GABAergic networks in the cerebral cortex. Using retrograde tracer injections in the subiculum, we identified a hippocampal population of ENK-expressing projection neurons. In situ hybridization for GAD shows that ENK-expressing cells are a small GABAergic subpopulation. Furthermore, by extracellular recording and juxtacellular labeling in vivo, we identified an ENK-expressing cell in stratum radiatum of the CA1 area by its complete axodendritic arborization and characteristic spike timing during network oscillations. The somatodendritic membrane was immunopositive for mGluR1
, and there was both a rich local axon in CA1 and subicular-projecting branches. The boutons showed cell-type- and layer-specific innervation, i.e., interneurons were the main targets in the alveus, both interneurons and pyramidal cell dendrites were innervated in the other layers, and interneurons were exclusive targets in the subiculum. Parvalbumin-, but not somatostatin-, calbindin-, or cholecystokinin-expressing interneurons were preferred synaptic targets. During network activity, the juxtacellularly labeled ENK-expressing cell was phase modulated throughout theta oscillations, but silenced during sharp-wave/ripple episodes. After these episodes the interneuron exhibited rebound activity of high-frequency spike bursts, presumably causing peptide release. The ENK-expressing interneurons innervating parvalbumin-positive interneurons might contribute to the organization of the sharp-wave/ripple episodes by decreased firing during and rebound activity after the ripple episodes, as well as to the coordination of activity between the CA1 and subicular areas during network oscillations.
Key words: interneuron; hippocampus; subiculum; in vivo; enkephalin; extracellular recordings
Received May 5, 2008; revised July 16, 2008; accepted Aug. 20, 2008.
Correspondence should be addressed to either Pablo Fuentealba or Peter Somogyi, Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford OX1 3TH, UK. Email: pablo.fuentealba{at}pharm.ox.ac.uk or Email: peter.somogyi{at}pharm.ox.ac.uk
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