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The Journal of Neuroscience, February 20, 2008, 28(8):1871-1881; doi:10.1523/JNEUROSCI.3948-07.2008

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Behavioral/Systems/Cognitive
Recurrent Synaptic Input and the Timing of Gamma-Frequency-Modulated Firing of Pyramidal Cells during Neocortical "UP" States

Kenji Morita,¹ Rita Kalra,² Kazuyuki Aihara,^3,4 and Hugh P. C. Robinson²

¹RIKEN Brain Science Institute, Wako 351-0198, Japan, ²Department of Physiology, Development, and Neuroscience, University of Cambridge, Cambridge CB2 3EG, United Kingdom, ³Institute of Industrial Science, University of Tokyo, Meguro, Tokyo 153-8505, Japan, and ⁴Aihara Complexity Modelling Project, Exploratory Research for Advanced Technology, Japan Science and Technology Corporation, Shibuya, Tokyo 151-0064, Japan

Correspondence should be addressed to Dr. Hugh P. C. Robinson, Department of Physiology, Development, and Neuroscience, University of Cambridge, Cambridge CB2 3EG, UK. Email: hpcr{at}cam.ac.uk

Gamma () oscillation, a hallmark of cortical activity during sensory processing and cognition, occurs during persistent, self-sustained activity or "UP" states, which are thought to be maintained by recurrent synaptic inputs to pyramidal cells. During neocortical "UP" states, excitatory regular spiking (RS) (pyramidal) cells and inhibitory fast spiking (FS) (basket) cells fire with distinct phase distributions relative to the oscillation in the local field potential. Evidence suggests that -modulated RS FS input serves to synchronize the interneurons and hence to generate -modulated FS RS drive. How RS RS recurrent input shapes both self-sustained activity and -modulated phasic firing, although, is unclear. Here, we investigate this by reconstructing -modulated synaptic input to RS cells using the conductance injection (dynamic clamp) technique in cortical slices. We find that, to show lifelike -modulated firing, RS cells require strongly -modulated, low-latency inhibitory inputs from FS cells but little or no -modulation from recurrent RS RS connections. We suggest that this demodulation of recurrent excitation, compared with inhibition, reflects several possible effects, including distributed propagation delays and integration of excitation over wider areas of cortex, and maximizes the capacity for representing information by the timing of recurrent excitation.

Key words: conductance injection; dynamic clamp; local field potential; regular-spiking; fast-spiking; synchronization

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Received June 22, 2007; revised Nov. 30, 2007; accepted Dec. 23, 2007.

Correspondence should be addressed to Dr. Hugh P. C. Robinson, Department of Physiology, Development, and Neuroscience, University of Cambridge, Cambridge CB2 3EG, UK. Email: hpcr{at}cam.ac.uk

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