Visual control of burst priming in the anesthetized lateral geniculate nucleus.

Thalamic relay cells fire bursts of action potentials. Once a long hyperpolarization "primes" (deinactivates) the T-type calcium channel, a depolarizing input will "trigger" a calcium spike with a burst of action potentials. During sleep, bursts are frequent, rhythmic, and nonvisual. Bursts have been observed in alert animals, and burst timing is known to carry visual information under light anesthesia. We extend this finding by showing that bursts without visual triggers are rare. Nevertheless, if the channel were primed at random with respect to the stimulus, then bursts would have the same visual significance as single spikes. We find, however, that visual signals influence when the channel is primed. First, natural time-varying stimuli evoke more bursts than white noise. Second, specific visual stimuli reproducibly elicit bursts, whereas others reliably elicit single spikes. Therefore, visual information is encoded by the selective tagging of some responses as bursts. The visual information attributable to visual priming (as distinct from the information attributable to visual triggering of the bursts) was two bits per burst on average. Although bursts are reportedly rare in alert animals, this must be investigated as a function of visual stimulus. Moreover, we propose methods to measure the extent of both visual triggering and visual priming of bursts. Whether or not bursts are rare, our methods could help determine whether bursts in alert animals carry a distinct visual signal.

A model of high-frequency oscillatory potentials in retinal ganglion cells.

High-frequency oscillatory potentials (HFOPs) have been recorded from ganglion cells in cat, rabbit, frog, and mudpuppy retina and in electroretinograms (ERGs) from humans and other primates. However, the origin of HFOPs is unknown. Based on patterns of tracer coupling, we hypothesized that HFOPs could be generated, in part, by negative feedback from axon-bearing amacrine cells excited via electrical synapses with neighboring ganglion cells. Computer simulations were used to determine whether such axon-mediated feedback was consistent with the experimentally observed properties of HFOPs. (1) Periodic signals are typically absent from ganglion cell PSTHs, in part because the phases of retinal HFOPs vary randomly over time and are only weakly stimulus locked. In the retinal model, this phase variability resulted from the nonlinear properties of axon-mediated feedback in combination with synaptic noise. (2) HFOPs increase as a function of stimulus size up to several times the receptive-field center diameter. In the model, axon-mediated feedback pooled signals over a large retinal area, producing HFOPs that were similarly size dependent. (3) HFOPs are stimulus specific. In the model, gap junctions between neighboring neurons caused contiguous regions to become phase locked, but did not synchronize separate regions. Model-generated HFOPs were consistent with the receptive-field center dynamics and spatial organization of cat alpha cells. HFOPs did not depend qualitatively on the exact value of any model parameter or on the numerical precision of the integration method. We conclude that HFOPs could be mediated, in part, by circuitry consistent with known retinal anatomy.