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Retinogeniculate Transmission in Wakefulness

Department of Cell Biology and Anatomy, Louisiana State University Health Sciences Center, New Orleans, Louisiana

Submitted 1 September 2006; accepted in final form 4 June 2007

Despite popular belief that the primary function of the thalamus is to "gate" sensory inputs by state, few studies have attempted to directly characterize the efficacy of such gating in the awake, behaving animal. I measured the efficacy of retinogeniculate transmission in the awake cat by taking advantage of the fact that many neurons in the lateral geniculate nucleus (LGN) are dominated by a single retinal input, and that this input produces a distinct event known as the S-potential. Retinal input failed to produce an LGN action potential half of the time. However, success or failure was powerfully tied to the recency of the S-potential. Short intervals tend to be successful and long intervals unsuccessful. For four of 12 neurons, the probability that a given S-potential could cause a spike exceeded 90% if that S-potential was preceded by an S-potential within the previous 10 ms (100 Hz). Whereas this temporal influence on efficacy has been demonstrated extensively in anesthetized animals, wakefulness is different in several ways. Overall efficacy is better in wakefulness than in anesthesia, the durations of facilitating effects are briefer in wakefulness, efficacy of long intervals is superior in wakefulness, and the temporal dependence can be briefly disrupted by altering background illumination. The last two observations may be particularly significant. Increased success at long intervals in wakefulness provides additional evidence that the spike code of the anesthetized animal is not the spike code of the awake animal. Altering retinogeniculate efficacy by altering visual conditions undermines the influence inter-S-potential interval might have in determining efficacy in the real world. Finally, S-potential amplitude, duration, and even slope are dynamic and systematic within wakefulness; providing further support that the S-potential is the extracellular signature of the retinal EPSP.