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J Neurophysiol (November 3, 2004). doi:10.1152/jn.00982.2004
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00982.2004v1
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Submitted on September 20, 2004
Accepted on October 31, 2004

Synchronization in Hybrid Neuronal Networks of the Hippocampal Formation

Theoden I. Netoff, Matthew I. Banks, Alan D. Dorval, Corey D. Acker, Julie S. Haas, Nancy Kopell, and John A. White*

* To whom correspondence should be addressed. E-mail: jwhite{at}bu.edu.

Understanding the mechanistic bases of neuronal synchronization is a current challenge in quantitative neuroscience. We studied this problem in two putative cellular pacemakers of the mammalian hippocampal theta rhythm: glutamatergic stellate cells (SCs) of the medial entorhinal cortex and GABAergic oriens-lacunosum-moleculare (O-LM) interneurons of hippocampal region CA1. We used two experimental methods. First, we measured changes in spike timing induced by artificial synaptic inputs applied to individual neurons. We then measured responses of free-running hybrid neuronal networks, consisting of biological neurons coupled (via dynamic clamp) to biological or virtual counterparts. Results from the single-cell experiments predicted network behaviors well, and are compatible with previous model-based predictions of how specific membrane mechanisms give rise to empirically measured synchronization behavior. Both cell types phase lock stably when connected via homogeneous excitatory-excitatory (E-E) or inhibitory-inhibitory (I-I) connections. Phase-locked firing is consistently synchronous for either cell type with E-E connections and nearly anti-synchronous with I-I connections. With heterogeneous connections (e.g., excitatory-inhibitory, as might be expected if members of a given population had heterogeneous connections involving intermediate interneurons), networks often settled into phase locking that was either stable or unstable, depending on the order of firing of the two cells in the hybrid network. Our results imply that excitatory SCs, but not inhibitory O-LM interneurons, are capable of synchronizing in phase via monosynaptic mutual connections of the biologically appropriate polarity. Results are largely independent of synaptic strength and synaptic kinetics, implying that our conclusions are robust and largely unaffected by synaptic plasticity.




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