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The Journal of Neuroscience, August 19, 2009, 29(33):10321-10334; doi:10.1523/JNEUROSCI.1703-09.2009

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Behavioral/Systems/Cognitive
Spatial Profile and Differential Recruitment of GABA_B Modulate Oscillatory Activity in Auditory Cortex

Anne-Marie M. Oswald,^1 * Brent Doiron,^1,2 * John Rinzel,^1,2 and Alex D. Reyes¹

¹Center for Neural Science and ²Courant Institute of Mathematical Sciences, New York University, New York, New York 10003

Correspondence should be addressed to Anne-Marie M. Oswald, Center for Neural Science, New York University, 4 Washington Place, Room 809, New York, NY 10003. Email: ammoswald{at}gmail.com

The interplay between inhibition and excitation is at the core of cortical network activity. In many cortices, including auditory cortex (ACx), interactions between excitatory and inhibitory neurons generate synchronous network gamma oscillations (30–70 Hz). Here, we show that differences in the connection patterns and synaptic properties of excitatory–inhibitory microcircuits permit the spatial extent of network inputs to modulate the magnitude of gamma oscillations. Simultaneous multiple whole-cell recordings from connected fast-spiking interneurons and pyramidal cells in L2/3 of mouse ACx slices revealed that for intersomatic distances <50 µm, most inhibitory connections occurred in reciprocally connected (RC) pairs; at greater distances, inhibitory connections were equally likely in RC and nonreciprocally connected (nRC) pairs. Furthermore, the GABA_B-mediated inhibition in RC pairs was weaker than in nRC pairs. Simulations with a network model that incorporated these features showed strong, gamma band oscillations only when the network inputs were confined to a small area. These findings suggest a novel mechanism by which oscillatory activity can be modulated by adjusting the spatial distribution of afferent input.

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Received April 6, 2009; revised July 3, 2009; accepted July 8, 2009.

Correspondence should be addressed to Anne-Marie M. Oswald, Center for Neural Science, New York University, 4 Washington Place, Room 809, New York, NY 10003. Email: ammoswald{at}gmail.com

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