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The Journal of Neuroscience, July 29, 2009, 29(30):9563-9574; doi:10.1523/JNEUROSCI.1397-09.2009

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Behavioral/Systems/Cognitive
Distinct Firing Patterns of Identified Basket and Dendrite-Targeting Interneurons in the Prefrontal Cortex during Hippocampal Theta and Local Spindle Oscillations

Katja Hartwich, Thomas Pollak, and Thomas Klausberger

Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, Oxford University, Oxford OX1 3TH, United Kingdom, and Center for Brain Research, Medical University of Vienna, 1090 Vienna, Austria

Correspondence should be addressed to Thomas Klausberger, Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, Oxford University, Oxford OX1 3TH, UK. Email: thomas.klausberger{at}pharm.ox.ac.uk

The medial prefrontal cortex is involved in working memory and executive control. However, the collective spatiotemporal organization of the cellular network has not been possible to explain during different brain states. We show that pyramidal cells in the prelimbic cortex fire synchronized to hippocampal theta and local spindle oscillations in anesthetized rats. To identify which types of interneurons contribute to the synchronized activity, we recorded and juxtacellularly labeled parvalbumin- and calbindin-expressing (PV+/CB+) basket cells and CB-expressing, PV-negative (CB+/PV–) dendrite-targeting interneurons during both network oscillations. All CB+/PV– dendrite-targeting cells strongly decreased their firing rate during hippocampal theta oscillations. Most PV+/CB+ basket cells fired at the peak of dorsal CA1 theta cycles, similar to prefrontal pyramidal cells. We show that pyramidal cells in the ventral hippocampus also fire around the peak of dorsal CA1 theta cycles, in contrast to previously reported dorsal hippocampal pyramidal cells. Therefore, prefrontal neurons might be driven by monosynaptic connections from the ventral hippocampus during theta oscillations. During prefrontal spindle oscillations, the majority of pyramidal cells and PV+/CB+ basket cells fired preferentially at the trough and early ascending phase, but CB+/PV– dendrite-targeting cells fired uniformly at all phases. We conclude that PV+/CB+ basket cells contribute to rhythmic responses of prefrontal pyramidal cells in relation to hippocampal and thalamic inputs and CB+/PV– dendrite-targeting cells modulate the excitability of dendrites and spines regardless of these field rhythms. Distinct classes of GABAergic interneuron in the prefrontal cortex contribute differentially to the synchronization of pyramidal cells during network oscillations.

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Received March 24, 2009; revised May 23, 2009; accepted June 22, 2009.

Correspondence should be addressed to Thomas Klausberger, Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, Oxford University, Oxford OX1 3TH, UK. Email: thomas.klausberger{at}pharm.ox.ac.uk

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