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The Journal of Neuroscience, February 21, 2007, 27(8):2058-2073; doi:10.1523/JNEUROSCI.2715-06.2007

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Behavioral/Systems/Cognitive
Synchronization of Electrically Coupled Pairs of Inhibitory Interneurons in Neocortex

Jaime G. Mancilla,^1 * Timothy J. Lewis,^2 * David J. Pinto,¹ John Rinzel,³ and Barry W. Connors¹

¹Department of Neuroscience, Division of Biology and Medicine, Brown University, Providence, Rhode Island 02912, ²Department of Mathematics, University of California, Davis, California 95616, and ³Center for Neural Science and Courant Institute of Mathematical Science, New York University, New York, New York 10003

Correspondence should be addressed to Jaime G. Mancilla at his present address: Department of Otolaryngology/Head and Neck Surgery, 1115 Bioinformatics Building, 130 Mason Farm Road, Campus Box 7070, University of North Carolina, Chapel Hill, NC 27599-7070. Email: mancilla{at}email.unc.edu

We performed a systematic analysis of phase locking in pairs of electrically coupled neocortical fast-spiking (FS) and low-threshold-spiking (LTS) interneurons and in a conductance-based model of a pair of FS cells. Phase–response curves (PRCs) were obtained for real interneurons and the model cells. We used PRCs and the theory of weakly coupled oscillators to make predictions about phase-locking characteristics of cell pairs. Phase locking and the robustness of phase-locked states to differences in intrinsic frequencies of cells were directly examined by driving interneuron pairs through a wide range of firing frequencies.

Calculations using PRCs accurately predicted that electrical coupling robustly synchronized the firing of interneurons over all frequencies studied (FS, 25–80 Hz; LTS, 10–30 Hz). The synchronizing ability of electrical coupling and the robustness of the phase-locked states were directly dependent on the strength of coupling but not on firing frequency. The FS cell model also predicted the existence of stable antiphase firing at frequencies below 30 Hz, but no evidence for stable antiphase firing was found using the experimentally determined PRCs or in direct measures of phase locking in pairs of interneurons.

Despite significant differences in biophysical properties of FS and LTS cells, their phase-locking behavior was remarkably similar. The wide spikes and shallow action potential afterhyperpolarizations of interneurons, compared with the model, prohibited antiphase behavior. Electrical coupling between cortical interneurons of the same type maintained robust synchronous firing of cell pairs for up to 10% heterogeneity in their intrinsic frequencies.

Key words: gap junctions; whisker barrel; oscillations; synchrony; FS cell; LTS cell; phase–response curves

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Received June 26, 2006; revised Dec. 28, 2006; accepted Dec. 29, 2006.

Correspondence should be addressed to Jaime G. Mancilla at his present address: Department of Otolaryngology/Head and Neck Surgery, 1115 Bioinformatics Building, 130 Mason Farm Road, Campus Box 7070, University of North Carolina, Chapel Hill, NC 27599-7070. Email: mancilla{at}email.unc.edu

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