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The Journal of Neuroscience, April 15, 1999, 19(8):2865-2875

Synchronized Paroxysmal Activity in the Developing Thalamocortical Network Mediated by Corticothalamic Projections and "Silent" Synapses

Peyman Golshani and Edward G. Jones

Center for Neuroscience, University of California, Davis, California 95616

In mouse thalamocortical slices in vitro, the potassium channel blocker 4-AP and GABA_A receptor antagonist bicuculline together induced spontaneous prolonged depolarizations in layer VI neurons from postnatal day 2 (P2), in ventroposterior nucleus neurons (VP) from P7, and in reticular nucleus neurons (RTN) from P8. Dual whole-cell recordings revealed that prolonged bursts were synchronized in layer VI, VP, and RTN. Bursts were present in cortex isolated from thalamus, but not in thalamus isolated from cortex, indicating that bursts originated in cortex and propagated to thalamus. Prolonged bursts were synchronized in layer VI when vertical cuts extended from pia mater through layers IV or V, but were no longer synchronized when cuts extended through layer VI and white matter.

In voltage-clamp recordings before P10, burst conductance of all three neuronal populations was dominated by the NMDA receptor-mediated conductance, and therefore synapses were "silent". In cortex and RTN, after P10, bursts were associated with strong AMPA/kainate receptor-mediated conductances, and synapses had become "functional"; silent synapses persisted in a large proportion of VP cells after P10.

Before P9, the NMDA receptor antagonist APV or the non-NMDA receptor antagonist CNQX blocked the prolonged bursts. After P9, CNQX continued to block the prolonged bursts, but APV merely shortened their duration.

Thus, NMDA receptor-based silent synapses are essential for paroxysmal corticothalamic activity during early postnatal development, and connections between layer VI neurons are sufficient for horizontal cortical synchronization.

Key words: ventroposterior nucleus; reticular nucleus; somatosensory cortex; NMDA receptor; cortical oscillations; paroxysmal activity

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Copyright © 1999 Society for Neuroscience  0270-6474/99/1982865-11$05.00/0

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