Postnatal development of synchronized network oscillations in the ferret dorsal lateral geniculate and perigeniculate nuclei

Abstract

Extracellular and intracellular recordings from slices of ferret dorsal lateral geniculate nucleus (LGNd) at postnatal ages P10-53 were performed to examine the postnatal development of spindle waves and the ability of block of GABAA receptors to alter these spindle waves into a slower, synchronous oscillation. As in prior studies in the adult, intracellular and extracellular recordings at ages P33-53 revealed robust spindle waves to be present in both the LGNd and perigeniculate nucleus (PGN). Intracellular recordings from thalamocortical relay cells in the A-laminae of the LGNd revealed that these cells received repetitive inhibitory postsynaptic potentials (IPSPs) at 6-9 Hz during the generation of spindle waves, and generated rebound low threshold Ca2+ spikes and bursts of 2-6 action potentials following each second or third IPSP. Intracellular recordings from the GABAergic neurons of the PGN at P33-53 revealed barrages of EPSPs that activated low threshold Ca2+ spikes and high frequency burst discharges of 2-10 action potentials during spindle wave generation. In contrast, full spindle waves were absent at ages prior to approximately P22 and spindle waves between the ages of P26 and approximately P30 were relatively weak and associated with only one or two action potentials per burst in both PGN neurons and LGNd relay cells. Bath application of the GABAA antagonist bicuculline methiodide at P41-53 resulted in a conversion of normal spindle waves into a marked 2-4 Hz oscillation in which the action potential firing of both thalamocortical relay and PGN neurons was greatly increased. In contrast, block of GABAA receptors prior to age P39 did not result in the generation of the slowed, 2-4 Hz network oscillation. Investigation of the electrophysiological properties of PGN neurons revealed that the postnatal development of spindle waves and bicuculline-induced slow oscillations were associated with an increase in the ability of PGN neurons to generate high frequency bursts of action potentials, suggesting that these changes in electrophysiological properties may contribute to the late development of synchronized oscillations in the ferret LGNd.