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The Journal of Neuroscience, June 29, 2005, 25(26):6175-6186; doi:10.1523/JNEUROSCI.0512-05.2005

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Behavioral/Systems/Cognitive
Bistable Network Behavior of Layer I Interneurons in Auditory Cortex

Elliott B. Merriam,1 Theoden I. Netoff,2 and Matthew I. Banks1

1Department of Anesthesiology, University of Wisconsin, Madison, Wisconsin 53706, and 2Department of Biomedical Engineering, Center for BioDynamics, Center for Memory and Brain, Boston University, Boston, Massachusetts 02215

GABAergic interneurons in many areas of the neocortex are mutually connected via chemical and electrical synapses. Previous computational studies have explored how these coupling parameters influence the firing patterns of interneuronal networks. These models have predicted that the stable states of such interneuronal networks will be either synchrony (near zero phase lag) or antisynchrony (phase lag near one-half of the interspike interval), depending on network connectivity and firing rates. In certain parameter regimens, the network can be bistable, settling into either stable state depending on the initial conditions. Here, we investigated how connectivity parameters influence spike patterns in paired recordings from layer I interneurons in brain slices from juvenile mice. Observed properties of chemical and electrical synapses were used to simulate connections between uncoupled cells via dynamic clamp. In uncoupled pairs, action potentials induced by constant depolarizing currents had randomly distributed phase differences between the two cells. When coupled with simulated chemical (inhibitory) synapses, however, these pairs exhibited a bimodal firing pattern, tending to fire either in synchrony or in antisynchrony. Combining electrical with chemical synapses, prolonging {tau}Decay of inhibitory connections, or increasing the firing rate of the network all resulted in enhanced stability of the synchronous state. Thus, electrical and inhibitory synaptic coupling constrain the relative timing of spikes in a two-cell network to, at most, two stable states, the stability and precision of which depend on the exact parameters of coupling.

Key words: inhibition; GABAA; gap junctions; synchrony; neocortex; anesthesia

Received Feb 7, 2005; revised May 12, 2005; accepted May 13, 2005.






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