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J Neurophysiol (November 3, 2004). doi:10.1152/jn.00983.2004
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Submitted on September 20, 2004
Accepted on November 3, 2004

A single-column thalamocortical network model exhibiting gamma oscillations, sleep spindles and epileptogenic bursts

Roger D. Traub1*, Diego Contreras2, Mark O. Cunningham3, Hilary Murray3, Fiona E. LeBeau3, Anita Roopun3, Andrea Bibbig1, W B. Wilent2, Michael Higley2, and Miles A. Whittington3

1 Physiology & Pharmacology, SUNY Downstate, Brooklyn, NY, USA
2 Neuroscience, University of Pennsylvania, Philadelphia, PA, USA
3 Biomedical Sciences, University of Leeds, Leeds, Yorkshire, United Kingdom

* To whom correspondence should be addressed. E-mail: roger.traub{at}downstate.edu.

In order the better to understand population phenomena in thalamocortical neuronal ensembles, we have constructed a preliminary network model with 3,560 multicompartment neurons (containing soma, branching dendrites, and a portion of axon). Types of neurons included superficial pyramids (with regular spiking [RS] and fast rhythmic bursting [FRB] firing behaviors); RS spiny stellates; fast spiking (FS) interneurons, with basket-type and axoaxonic types of connectivity, and located in superficial and deep cortical layers; low threshold spiking (LTS) interneurons, that contacted principal cell dendrites; deep pyramids, that could have RS or intrinsic bursting (IB) firing behaviors, and endowed either with non-tufted apical dendrites or with long tufted apical dendrites; thalamocortical relay (TCR) cells; and nucleus reticularis (nRT) cells. To the extent possible, both electrophysiology and synaptic connectivity were based on published data, although many arbitrary choices were necessary. In addition to synaptic connectivity (via AMPA/kainate, NMDA and GABAA receptors), we also included electrical coupling between dendrites of interneurons, nRT cells, and TCR cells, and - in various combinations - electrical coupling between the proximal axons of certain cortical principal neurons. Our network model replicates several observed population phenomena, including a) persistent gamma oscillations; b) thalamocortical sleep spindles; c) series of synchronized population bursts, resembling electrographic seizures; d) isolated double population bursts with superimposed very fast oscillations (>100 Hz, 'VFO'); e) spike-wave, polyspike-wave and fast runs (~10 Hz). We show that epileptiform bursts, including double and multiple bursts, containing VFO, occur in rat auditory cortex in vitro, in the presence of kainate, when both GABAA and GABAB receptors are blocked. Electrical coupling between axons appears necessary (as reported previously) for persistent gamma, and additionally plays a role in the detailed shaping of epileptogenic events. The degree of recurrent synaptic excitation between spiny stellate cells, and their tendency to fire throughout multiple bursts, also appears critical in shaping epileptogenic events.




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