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The Journal of Neuroscience, August 15, 2007, 27(33):8790-8804; doi:10.1523/JNEUROSCI.1847-07.2007

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Behavioral/Systems/Cognitive
Neuronal Diversity in GABAergic Long-Range Projections from the Hippocampus

Shozo Jinno,¹ Thomas Klausberger,^1,2 Laszlo F. Marton,^1,3 Yannis Dalezios,^1,4,5 J. David B. Roberts,¹ Pablo Fuentealba,¹ Eric A. Bushong,¹ Darrell Henze,⁶ György Buzsáki,⁶ and Peter Somogyi¹

¹Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, Oxford University, Oxford OX1 3TH, United Kingdom, ²Center for Brain Research, Medical University of Vienna, 1090 Vienna, Austria, ³Neural Systems Research Group, Faculty of Engineering, Sapientia-Hungarian University of Transylvania, RO-540485 Targu Mures, Romania, ⁴Faculty of Medicine, University of Crete, 71003 Heraklion, Greece, ⁵Institute of Applied and Computational Mathematics, Foundation for Research and Technology-Hellas, GR-711 10 Heraklion, Greece, and ⁶Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey 07102-1811

Correspondence should be addressed to any of the following: Dr. Shozo Jinno, Department of Anatomy and Neurobiology, Graduate School of Medical Sciences, Kyushu University, Maidashi 3-1-1, Higashi-ku, Fukuoka 812-8582, Japan, Email: sjnno{at}med.kyushu-u.ac.jp; Drs. Thomas Klausberger or Peter Somogyi, Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, Oxford University, Oxford OX1 3TH, UK, E-mail: Email: thomas.klausberger{at}pharmacology.oxford.ac.uk or Email: peter.somogyi{at}pharmacology.oxford.ac.uk

The formation and recall of sensory, motor, and cognitive representations require coordinated fast communication among multiple cortical areas. Interareal projections are mainly mediated by glutamatergic pyramidal cell projections; only few long-range GABAergic connections have been reported. Using in vivo recording and labeling of single cells and retrograde axonal tracing, we demonstrate novel long-range GABAergic projection neurons in the rat hippocampus: (1) somatostatin- and predominantly mGluR1-positive neurons in stratum oriens project to the subiculum, other cortical areas, and the medial septum; (2) neurons in stratum oriens, including somatostatin-negative ones; and (3) trilaminar cells project to the subiculum and/or other cortical areas but not the septum. These three populations strongly increase their firing during sharp wave-associated ripple oscillations, communicating this network state to the septotemporal system. Finally, a large population of somatostatin-negative GABAergic cells in stratum radiatum project to the molecular layers of the subiculum, presubiculum, retrosplenial cortex, and indusium griseum and fire rhythmically at high rates during theta oscillations but do not increase their firing during ripples. The GABAergic projection axons have a larger diameter and thicker myelin sheet than those of CA1 pyramidal cells. Therefore, rhythmic IPSCs are likely to precede the arrival of excitation in cortical areas (e.g., subiculum) that receive both glutamatergic and GABAergic projections from the CA1 area. Other areas, including the retrosplenial cortex, receive only rhythmic GABAergic CA1 input. We conclude that direct GABAergic projections from the hippocampus to other cortical areas and the septum contribute to coordinating oscillatory timing across structures.

Key words: cerebral cortex; inhibition; interneuron; oscillation; rhythm; axon

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Received April 23, 2007; revised June 1, 2007; accepted June 11, 2007.

Correspondence should be addressed to any of the following: Dr. Shozo Jinno, Department of Anatomy and Neurobiology, Graduate School of Medical Sciences, Kyushu University, Maidashi 3-1-1, Higashi-ku, Fukuoka 812-8582, Japan, Email: sjnno{at}med.kyushu-u.ac.jp; Drs. Thomas Klausberger or Peter Somogyi, Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, Oxford University, Oxford OX1 3TH, UK, E-mail: Email: thomas.klausberger{at}pharmacology.oxford.ac.uk or Email: peter.somogyi{at}pharmacology.oxford.ac.uk

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