Retinal output changes qualitatively with every change in ambient illuminance

Tikidji-Hamburyan, Alexandra; Reinhard, Katja; Seitter, Hartwig; Հովհաննիսյան, Անահիտ; Procyk, Christopher A.; Allen, Annette E.; Schenk, Martin; Lucas, Robert J.; Münch, Thomas A.

doi:10.1038/nn.3891

Cited by 119 publications

(137 citation statements)

References 59 publications

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“…As recently shown, this method of classification has the important advantage of returning consistent results across irradiance levels, whereas the ON-OFF profile of responses to simple steps is labile (34). Accordingly, units segregated into consistent ON or OFF types across irradiance levels.…”

Section: Resultsmentioning

confidence: 97%

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

Storchi

Milosavljevic

Eleftheriou

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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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

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Section: Resultsmentioning

confidence: 97%

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

Storchi

Milosavljevic

Eleftheriou

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Recent studies illustrate, albeit qualitatively, how little we understand about the behaviors of some cell types in response to changing ambient light intensities. Across ~100-fold changes in background light level, some ON or OFF cells seemed to alter their identities and generate ON–OFF responses (Pearson & Kerschensteiner 2015, Tikidji-Hamburyan et al 2015). These effects were also observed in vivo.…”

Section: Resultsmentioning

confidence: 99%

Functional Circuitry of the Retina

Demb

Singer

2015

Annu. Rev. Vis. Sci.

161

131

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The mammalian retina is an important model system for studying neural circuitry: Its role in sensation is clear, its cell types are relatively well defined, and its responses to natural stimuli—light patterns—can be studied in vitro. To solve the retina, we need to understand how the circuits pre-synaptic to its output neurons, ganglion cells, divide the visual scene into parallel representations to be assembled and interpreted by the brain. This requires identifying the component interneurons and understanding how their intrinsic properties and synapses generate circuit behaviors. Because the cellular composition and fundamental properties of the retina are shared across species, basic mechanisms studied in the genetically modifiable mouse retina apply to primate vision. We propose that the apparent complexity of retinal computation derives from a straightforward mechanism—a dynamic balance of synaptic excitation and inhibition regulated by use-dependent synaptic depression—applied differentially to the parallel pathways that feed ganglion cells.

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“…Our study was the first to demonstrate in awake, behaving animals a substantial OFF-cell dominance not only in neural sensitivity, but also in basic physiological properties such as spontaneous activity, peak activity, response sustainability and, to some extent, response latency. Importantly, changes in ambient illumination could potentially lead to changes in LGN ON and OFF neural responses (Farrow et al 2013;Pandarinath et al 2010;Tikidji-Hamburyan et al 2015). The background luminance for stimulus presentation was fixed at ϳ15 cd/m 2 for all of our experiments, which is in the low photopic range.…”

Section: Neural Sensitivitymentioning

confidence: 99%

The functional asymmetry of ON and OFF channels in the perception of contrast

Jiang

Purushothaman

Casagrande

2015

Journal of Neurophysiology

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-To fully understand the relationship between perception and single neural responses, one should take into consideration the early stages of sensory processing. Few studies, however, have directly examined the neural underpinning of visual perception in the lateral geniculate nucleus (LGN), only one synapse away from the retina. In this study we recorded from LGN parvocellular (P) ON-center and OFF-center neurons while monkeys either passively viewed or actively detected a full range of contrasts. We found that OFF neurons were more sensitive in detecting negative contrasts than ON neurons were in detecting positive contrasts. Also, OFF neurons had higher spontaneous activities, higher peak response amplitudes, and were more sustained than ON neurons in their contrast responses. Puzzlingly, OFF neurons failed to show any significant correlations with the monkeys' perceptual choices, despite their greater contrast sensitivities. If, however, choice probabilities were calculated from interspike intervals instead of spike counts (thus taking into account the higher firing rates of OFF neurons), OFF neurons but not ON neurons were significantly correlated with behavioral choices. Taken together, these results demonstrate in awake, behaving animals that: 1) the ON and OFF pathways do not simply mirror each other in their functionality but instead carry qualitatively different types of information, and 2) the responses of ON and OFF neurons can be correlated with perceptual choices even in the absence of physical stimuli and interneuronal correlations. lateral geniculate nucleus; ON-center cell; OFF-center cell; contrast detection; choice probability EARLY PSYCHOPHYSICAL STUDIES indicated that separate channels underlie our perception of brightness (i.e., positive contrasts, or luminance increments) and darkness (i.e., negative contrasts, or luminance decrements), respectively

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Retinal output changes qualitatively with every change in ambient illuminance

Cited by 119 publications

References 59 publications

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

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

Functional Circuitry of the Retina

The functional asymmetry of ON and OFF channels in the perception of contrast

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