Visual Control of Burst Priming in the Anesthetized Lateral Geniculate Nucleus

Abstract

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.

Transmission of Spike Trains at the Retinogeniculate Synapse

“…Therefore, the bursts that we observed were not related to transitions between sleep and wakefulness. Another potential role for bursts is to signal salient or novel features in the visual environment Reinagel et al, 1999;Lesica and Stanley, 2004;Alitto et al, 2005;Denning and Reinagel, 2005). This concept is appealing because quiescent LGN cells are likely to be transiently activated by such stimuli.…”

Recoding of Sensory Information across the Retinothalamic Synapse

“…We disregarded the third case (see controls in supplement C, available at www.jneurosci. org as supplemental material) because there are very few anonymous spikes ; typically, these are produced during bursts (Wang et al, 2007), which occur reliably but rarely during vision (Guido and Weyand, 1995;Usrey et al, 1999) and are better driven by naturalistic stimuli than by noise (Lesica and Stanley, 2004;Denning and Reinagel, 2005). Thus, we were able to model transmission as a binary selection (i.e., relayed or not) of the retinal spike train (Fig.…”

Luminance-Evoked Inhibition in Primary Visual Cortex: A Transient Veto of Simultaneous and Ongoing Response

“…However, the neural substrate that mediates luminance-evoked suppression of cortical response remains unresolved. Lateral geniculate neurons generate transient responses to changes in luminance (Schiller, 1968;Sherman, 2001;Martinez-Conde et al, 2002;Denning and Reinagel, 2005), raising the possibility that cortical response suppression arises from a reduction in the activity of excitatory feedforward inputs. However, evidence that visual masking phenomena exhibit interocular transfer (a masking stimulus presented to one eye can mask the appearance of a stimulus presented to the other eye) suggests that luminance-evoked suppression may depend on intracortical circuits, perhaps reflecting the preferential recruitment of cortical inhibitory neurons (Kolers and Rosner, 1960;Schiller, 1965;Macknik and Martinez-Conde, 2004).…”

“…One interesting possibility is suggested by the observation that large-scale changes in luminance frequently evoke high-frequency burst discharges in LGN neurons (Schiller, 1968;Ramcharan et al, 2001;Sherman, 2001;Lesica and Stanley, 2004;Alitto et al, 2005;Denning and Reinagel, 2005). Similar burst discharges in somatosensory thalamus have been shown to be effective in driving the responses of layer 4 cortical inhibitory neurons (Swadlow and Gusev, 2001).…”