Synaptic mechanisms of temporal diversity in the lateral geniculate nucleus of the thalamus

The lateral geniculate nucleus (LGN) contains a unique and numerous class of cells called lagged cells, which introduce a time delay into the neural signal provided to cortex. Previous studies have shown that this delay is dependent on GABA(A) receptors within the LGN. Furthermore, lagged cells have distinct integrative properties with a slower rising, more sustained, and overall lower firing rates than nonlagged cells. We have recorded intracellularly from lagged cells in the cat LGN and found a unique property of their retinal inputs that underlies both their temporal and integrative visual response properties. Lagged cell EPSPs, which often derive from a single retinal input, have smaller amplitudes, repolarize more quickly, and are followed by a Cl(-)-dependent hyperpolarization compared with nonlagged cells. The Cl(-)-dependent hyperpolarization sums early in the visual response generating a powerful synaptic inhibition that coincides with the peak frequency of retinal input and delays the spike response in lagged cells. The hyperpolarization subsides rapidly over ∼20-40 ms allowing for slow summation of the retinal input leading to the visual spike response. Given the tight association of single retinal EPSPs and the following inhibition, we propose that both functional properties result from the triadic circuitry prevalent in the LGN and particularly prominent in lagged X-cells. Thus, our results show for the first time a dynamic interaction of retinal excitation and fast feedforward inhibition that determines the integrative properties and the delay in firing of lagged cells.