Spatial modulation of dark versus bright stimulus responses in the mouse visual system

Williams, Byron; Rosario, Joseph Del; Muzzu, Tomaso; Peelman, Kayla; Coletta, Stefano; Bichler, Edyta K.; Speed, Anderson; Meyer-Baese, Lisa; Saleem, Aman B.; Haider, Bilal

doi:10.1016/j.cub.2021.06.094

Cited by 29 publications

(24 citation statements)

References 55 publications

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“…In fact, several studies have shown that primary visual neurons of primates and cats respond more strongly to black than to white spots and oriented bars ( Liu and Yao, 2014 ; Xing et al, 2010 ; Yeh et al, 2009 ). A very recent study has shown that this is the case also for the central visual field of mice, although in the periphery OFF and ON response are more balanced ( Williams et al, 2021 ). Indeed, the asymmetry begins already in the retina where there are more OFF cells than ON cells ( Ratliff et al, 2010 ).…”

Section: Discussionmentioning

confidence: 90%

“…Unlike two- or four-point statistics,

statistics change contrast under a sign change (namely, positive

values correspond to white triangular patterns on a black background, and negative

values correspond to black triangular patterns on a white background). On the other hand, dominance of OFF responses (elicited by dark spots on a light background) has been reported in mammals, including primates, cats, and rodents ( Ratliff et al, 2010 ; Liu and Yao, 2014 ; Xing et al, 2010 ; Yeh et al, 2009 ; Williams et al, 2021 ). Therefore we reasoned that if rats, unlike humans, were to have a different sensitivity to positive and negative

values, the sensitivity to negative

would be the higher of the two.…”

Section: Methodsmentioning

confidence: 99%

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Rat sensitivity to multipoint statistics is predicted by efficient coding of natural scenes

Caramellino

Piasini

Buccellato

et al. 2021

eLife

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Efficient processing of sensory data requires adapting the neuronal encoding strategy to the statistics of natural stimuli. Previously, in Hermundstad et al., 2014, we showed that local multipoint correlation patterns that are most variable in natural images are also the most perceptually salient for human observers, in a way that is compatible with the efficient coding principle. Understanding the neuronal mechanisms underlying such adaptation to image statistics will require performing invasive experiments that are impossible in humans. Therefore, it is important to understand whether a similar phenomenon can be detected in animal species that allow for powerful experimental manipulations, such as rodents. Here we selected four image statistics (from single- to four-point correlations) and trained four groups of rats to discriminate between white noise patterns and binary textures containing variable intensity levels of one of such statistics. We interpreted the resulting psychometric data with an ideal observer model, finding a sharp decrease in sensitivity from two- to four-point correlations and a further decrease from four- to three-point. This ranking fully reproduces the trend we previously observed in humans, thus extending a direct demonstration of efficient coding to a species where neuronal and developmental processes can be interrogated and causally manipulated.

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Section: Discussionmentioning

confidence: 90%

“…Unlike two- or four-point statistics,

statistics change contrast under a sign change (namely, positive

values correspond to white triangular patterns on a black background, and negative

values, the sensitivity to negative

would be the higher of the two.…”

Section: Methodsmentioning

confidence: 99%

Rat sensitivity to multipoint statistics is predicted by efficient coding of natural scenes

Caramellino

Piasini

Buccellato

et al. 2021

eLife

View full text Add to dashboard Cite

show abstract

“…In fact, several studies have shown that primary visual neurons of primates and cats respond more strongly to black than to white spots and oriented bars (Liu and Yao 2014;Xing, Yeh, and Shapley 2010;Yeh, Xing, and Shapley 2009). A very recent study has shown that this is the case also for the central visual field of mice, although in the periphery OFF and ON response are more balanced (Williams et al 2021). Indeed, the asymmetry begins already in the retina where there are more OFF cells than ON cells (Ratliff et al 2010).…”

Section: Discussionmentioning

confidence: 95%

“…Unlike 2-or 4-point statistics, θ statistics change contrast under a sign change (namely, positive θ values correspond to white triangular patterns on a black background, and negative θ values correspond to black triangular patterns on a white background). On the other hand, dominance of OFF responses (elicited by dark spots on a light background) has been reported in mammals, including primates, cats, and rodents (Ratliff et al 2010;Liu and Yao 2014;Xing, Yeh, and Shapley 2010;Yeh, Xing, and Shapley 2009;Williams et al 2021). Therefore we reasoned that if rats, unlike humans, were to have a different sensitivity to positive and negative θ values, the sensitivity to negative θ would be the higher of the two.…”

Section: Choice Of Image Statistics To Be Used In the Experimentsmentioning

confidence: 99%

Rat sensitivity to multipoint statistics is predicted by efficient coding of natural scenes

Caramellino

Piasini

Buccellato

et al. 2021

Preprint

View full text Add to dashboard Cite

Efficient processing of sensory data requires adapting the neuronal encoding strategy to the statistics of natural stimuli. Humans, for instance, are most sensitive to multipoint correlations that vary the most across natural images. Here we show that rats possess the same sensitivity ranking to multipoint statistics as humans, thus extending a classic demonstration of efficient coding to a species where neuronal and developmental processes can be interrogated and causally manipulated.

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“…In the visual system, neural channels transmitting information about luminance increases (ON) and decreases (OFF) constitute one key example of parallel pathways requiring integration (Chen et al, 2017; Williams et al, 2021). Although luminance information is segregated between ON and OFF cells early on in the retina of insects and mammals, real world scenes involve a mix of both (Leonhardt et al, 2016; Chen et al, 2019; Mazade et al, 2019; Mulholland and Smith, 2021).…”

Section: Introductionmentioning

confidence: 99%

Contrast-polarity specific mapping optimizes neuronal computation for collision detection

Dewell

Zhu

Eisenbrandt

et al. 2022

Preprint

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Neurons receive information through their synaptic inputs, but the functional significance of how those inputs are mapped on to a cell’s dendrites remains unclear. We studied this question in a grasshopper visual neuron that tracks approaching objects and triggers escape behavior before an impending collision. In response to black approaching objects, the neuron receives OFF excitatory inputs that form a retinotopic map of the visual field onto compartmentalized, distal dendrites. Subsequent processing of these OFF inputs by active membrane conductances allows the neuron to discriminate the spatial coherence of such stimuli. In contrast, we show that ON excitatory synaptic inputs activated by white approaching objects map in a random manner onto a more proximal dendritic field of the same neuron. This random synaptic arrangement results in the neuron’s inability to discriminate the coherence of white approaching stimuli. Yet, the neuron retains the ability to discriminate stimulus coherence for checkered stimuli of mixed ON/OFF polarity. The coarser mapping and processing of ON stimuli thus has a minimal impact, while reducing the total energetic cost of the circuit. Further, we show that these differences in ON/OFF neuronal processing are behaviorally relevant, being tightly correlated with the animal’s escape behavior to light and dark stimuli of variable coherence. Our results show that the synaptic mapping of excitatory inputs affects the fine stimulus discrimination ability of single neurons and document the resulting functional impact on behavior.

show abstract

Spatial modulation of dark versus bright stimulus responses in the mouse visual system

Cited by 29 publications

References 55 publications

Rat sensitivity to multipoint statistics is predicted by efficient coding of natural scenes

Rat sensitivity to multipoint statistics is predicted by efficient coding of natural scenes

Rat sensitivity to multipoint statistics is predicted by efficient coding of natural scenes

Contrast-polarity specific mapping optimizes neuronal computation for collision detection

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