Melanopsin-driven increases in maintained activity enhance thalamic visual response reliability across a simulated dawn

Abstract

Twice a day, at dawn and dusk, we experience gradual but very high amplitude changes in background light intensity (irradiance). Although we perceive the associated change in environmental brightness, the representation of such very slow alterations in irradiance by the early visual system has been little studied. Here, we addressed this deficit by recording electrophysiological activity in the mouse dorsal lateral geniculate nucleus under exposure to a simulated dawn. As irradiance increased we found a widespread enhancement in baseline firing that extended to units with ON as well as OFF responses to fast luminance increments. This change in baseline firing was equally apparent when the slow irradiance ramp appeared alone or when a variety of higher-frequency artificial or natural visual stimuli were superimposed upon it. Using a combination of conventional knockout, chemogenetic, and receptor-silent substitution manipulations, we continued to show that, over higher irradiances, this increase in firing originates with inner-retinal melanopsin photoreception. At the single-unit level, irradiance-dependent increases in baseline firing were strongly correlated with improvements in the amplitude of responses to higher-frequency visual stimuli. This in turn results in an up to threefold increase in single-trial reliability of fast visual responses. In this way, our data indicate that melanopsin drives a generalized increase in dorsal lateral geniculate nucleus excitability as dawn progresses that both conveys information about changing background light intensity and increases the signal:noise for fast visual responses. melanopsin | irradiance | neural coding | silent substitution | DREADD

Modulation of Fast Narrowband Oscillations in the Mouse Retina and dLGN According to Background Light Intensity

“…To this end, we exposed freely moving mice carrying electrodes implanted into the dLGN to 10 s steps in background light intensity (from ''dim,'' 11.9 log 10 photons/cm 2 /s, to ''bright,'' 15.1 log 10 photons/cm 2 /s). The irradiance step induced a substantial increase in the maintained firing rate of the dLGN ( Figure 1B; normalized population response), as reported previously in anesthetized mice (Storchi et al, 2015). The dLGN activity at high irradiance was also characterized by fast periodic spiking ( Figure 1C).…”

“…The daylight ramp stimulus is known to also elicit a widespread increase in firing rate of dLGN units (Storchi et al, 2015), and indeed there was a positive correlation between firing rate and normalized peak power in these recordings ( Figure S2B). However, the increase in the power of narrowband oscillations across the ramp was apparent even after correcting for differences in firing rate ( Figures S2C and S2D), confirming that these are at least partially separable phenomena.…”

“…To address this question, we used a ramp stimulus previously shown to allow an effective separation of the contribution of these different classes of photoreceptors to irradiancedependent increases in maintained firing rate (Storchi et al, 2015). This stimulus features a spatially diffuse, very gradual 1,0003 increase in irradiance (rise time = 13 min).…”

“…We have previously described a variant of the daylight ramp that is selectively deficient in those wavelengths to which melanopsin is most sensitive (Storchi et al, 2015), with the result that it is predicted to appear $103 dimmer for melanopsin across the whole ramp, but approximately isoluminant for cones (see Supplemental Experimental Procedures). We therefore expect any response driven by melanopsin to be less engaged by this ''mel low'' ramp.…”

An evolving view of retinogeniculate transmission

“…The continually expanding toolbox for interrogating diversity in neuronal circuits is already uncovering nuances in the contribution of different RGC types to TC neuron function (Storchi et al, 2015; Denman et al, 2016). Advances in methods for labeling, activating, and measuring the activity of different neuronal populations that have been deployed extensively in mice may also reveal underappreciated subtleties of retinogeniculate transmission in other species (Scholl et al, 2013; Zaltsman et al, 2015; Zeater et al, 2015; Suresh et al, 2016).…”