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The Journal of Neuroscience, April 5, 2006, 26(14):3646-3655; doi:10.1523/JNEUROSCI.4605-05.2006

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Behavioral/Systems/Cognitive
Correlation-Induced Synchronization of Oscillations in Olfactory Bulb Neurons

Roberto F. Galán,^1,3 * Nicolas Fourcaud-Trocmé,^2,3 * G. Bard Ermentrout,^2,3 and Nathaniel N. Urban^1,3

¹Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, ²Department of Mathematics, University of Pittsburgh, Pittsburgh, Pennsylvania 15260, and ³Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania 15213

Correspondence should be addressed to Nathaniel N. Urban, Department of Biological Sciences, Carnegie Mellon University, 4400 Fifth Avenue, Pittsburgh, PA 15213. Email: nurban{at}cmu.edu

Oscillations are a common feature of odor-evoked and spontaneous activity in the olfactory system in vivo and in vitro and are thought to play an important role in information processing and memory in a variety of brain areas. Theoretical and experimental studies have described several mechanisms by which oscillations can be generated and synchronized. Here, we investigate the hypothesis that correlated noisy inputs are able to generate synchronous oscillations in olfactory bulb mitral cells in vitro. We consider several alternative mechanisms and conclude that olfactory bulb synchronous oscillations are likely to arise because of the response of uncoupled oscillating neurons to aperiodic but correlated inputs. This mechanism has been described theoretically, but we provide the first experimental evidence that such a mechanism may underlie synchronization in real neurons. In physiological experiments, we show that this mechanism can generate gamma-band oscillations in populations of olfactory bulb mitral cells. This mechanism synchronizes oscillatory firing by using shared fast fluctuations in stochastic inputs across neurons, without requiring any synaptic or electrical coupling. We discuss the properties and limitations of synchronization by this mechanism and suggest that it may underlie fast oscillations in many brain areas.

Key words: inhibition; olfactory bulb; synchronization; slice; oscillator; mitral cell

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Received Oct. 27, 2005; revised Feb. 15, 2006; accepted Feb. 17, 2006.

Correspondence should be addressed to Nathaniel N. Urban, Department of Biological Sciences, Carnegie Mellon University, 4400 Fifth Avenue, Pittsburgh, PA 15213. Email: nurban{at}cmu.edu

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