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The Journal of Neuroscience, September 27, 2006, 26(39):9923-9934; doi:10.1523/JNEUROSCI.1580-06.2006

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Behavioral/Systems/Cognitive
Synaptic Currents in Anatomically Identified CA3 Neurons during Hippocampal Gamma Oscillations In Vitro

Iris Oren,¹ Edward O. Mann,¹ Ole Paulsen,¹ and Norbert Hájos²

¹Department of Physiology, Anatomy, and Genetics, University of Oxford, Oxford OX1 3PT, United Kingdom, and ²Department of Cellular and Network Neurobiology, Institute of Experimental Medicine, Hungarian Academy of Sciences, H-1450 Budapest, Hungary

Correspondence should be addressed to Dr. Ole Paulsen, Department of Physiology, Anatomy and Genetics, University of Oxford, Sherrington Building, Parks Road, Oxford OX1 3PT, UK. Email: ole.paulsen{at}physiol.ox.ac.uk

Gamma-frequency oscillations are prominent during active network states in the hippocampus. An intrahippocampal gamma generator has been identified in the CA3 region. To better understand the synaptic mechanisms involved in gamma oscillogenesis, we recorded action potentials and synaptic currents in distinct types of anatomically identified CA3 neurons during carbachol-induced (20–25 µM) gamma oscillations in rat hippocampal slices. We wanted to compare and contrast the relationship between excitatory and inhibitory postsynaptic currents in pyramidal cells and perisomatic-targeting interneurons, cell types implicated in gamma oscillogenesis, as well as in other interneuron subtypes, and to relate synaptic currents to the firing properties of the cells. We found that phasic synaptic input differed between cell classes. Most strikingly, the dominant phasic input to pyramidal neurons was inhibitory, whereas phase-coupled perisomatic-targeting interneurons often received a strong phasic excitatory input. Differences in synaptic input could account for some of the differences in firing rate, action potential phase precision, and mean action potential phase angle, both between individual cells and between cell types. There was a strong positive correlation between the ratio of phasic synaptic excitation to inhibition and firing rate over all neurons and between the phase precision of excitation and action potentials in interneurons. Moreover, mean action potential phase angle correlated with the phase of the peak of the net-estimated synaptic reversal potential in all phase-coupled neurons. The data support a recurrent mechanism of gamma oscillations, whereby spike timing is controlled primarily by inhibition in pyramidal cells and by excitation in interneurons.

Key words: gamma oscillation; interneuron; synaptic; cholinergic; hippocampus; rat

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Received April 12, 2006; revised July 6, 2006; accepted Aug. 15, 2006.

Correspondence should be addressed to Dr. Ole Paulsen, Department of Physiology, Anatomy and Genetics, University of Oxford, Sherrington Building, Parks Road, Oxford OX1 3PT, UK. Email: ole.paulsen{at}physiol.ox.ac.uk

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