Predictive encoding of motion begins in the primate retina

Liu, Belle; Hong, Arthur; Manookin, Michael B.

doi:10.1038/s41593-021-00899-1

Cited by 33 publications

(31 citation statements)

References 63 publications

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“…OPEN ACCESS of contrast-mediated motion signals ('second-order motion') [32] and to detecting subtle fixational eye movements [33,34]. Combining rectification of bipolar-cell subunit signals with gap-junction coupling between bipolar cells can further enhance sensitivity to specific motion signals [24,35], which is hypothesized to enhance the information about future locations of continuously moving objects [36]. Even for ON-OFF direction-selective ganglion cells, where much of the computation of directionality occurs in the presynaptic starburst amacrine cells, the crucial integration of excitatory and inhibitory inputs occurs locally along the dendritic tree of the ganglion cell, providing a subunit architecture to the motion processing [37,38].…”

Section: Trends In Neurosciencesmentioning

confidence: 99%

Retinal receptive-field substructure: scaffolding for coding and computation

Zapp

Nitsche

Gollisch

2022

Trends in Neurosciences

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Section: Trends In Neurosciencesmentioning

confidence: 99%

Retinal receptive-field substructure: scaffolding for coding and computation

Zapp

Nitsche

Gollisch

2022

Trends in Neurosciences

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“…Recent work in primate demonstrated that electrical coupling of retinal bipolar cells enabled predictive coding at the ganglion cell level by generating specific sensitivity to spatial correlations in incoming stimuli (Liu et al, 2021). Bipolar cells in mouse retina, too, have been shown to be electrically coupled, and therefore may contribute to the ganglion cells' phase-advanced response through predictive coding.…”

Section: The Role Of Gap Junction Coupling In Phase Advancingmentioning

confidence: 99%

Phase Advancing Is a Common Property of Multiple Neuron Classes in the Mouse Retina

DePiero

Borghuis

2022

eNeuro

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Behavioral interactions with moving objects are challenged by response latencies within the sensory and motor nervous systems. In vision, the combined latency from phototransduction and synaptic transmission from the retina to central visual areas amounts to 50-100 ms, depending on stimulus conditions. Time required for generating appropriate motor output adds to this latency and further compounds the behavioral delay. Neuronal adaptations that help counter sensory latency within the retina have been demonstrated in some species, but how general these specializations are, and where in the circuitry they originate, remains unclear. To address this, we studied the timing of object motion-evoked responses at multiple signaling stages within the mouse retina using two-photon fluorescence calcium and glutamate imaging, targeted wholecell electrophysiology, and computational modeling. We found that both ON and OFFtype ganglion cells, as well as the bipolar cells that innervate them, temporally advance the position encoding of a moving object and so help counter the inherent signaling delay in the retina. Model simulations show that this predictive capability is a direct consequence of the spatial extent of the cells' linear visual receptive field, with no apparent specialized circuits that help predict beyond it. Significance StatementSignal transduction and synaptic transmission within sensory signaling pathways costs time. Not a lot of time, just tens to a few hundred milliseconds depending on the sensory system, but enough to challenge fast behavioral interactions under dynamic stimulus conditions, like catching a moving fly. To counter neuronal delays, nervous systems of many species use anticipatory mechanisms. One such mechanism in the mammalian visual system helps predict the future position of a moving target through a process called phase advancing. Here we ask for functionally diverse neuron populations in the mouse retina how common is phase advancing and demonstrate that it is common and generated at multiple signaling stages.

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“…However, recent anatomical studies have revealed that parasol RGCs are too sparsely distributed, and they have receptive fields that are too large to support high acuity achromatic vision ( Masri et al, 2020 ; Patterson et al, 2020 ). Moreover, their receptive field structure, bipolar cell circuitry ( Patterson et al, 2020 ), projection to the magnocellular (M) pathway and dorsal stream, and response characteristics are well suited for mediating visually guided movements of our forelimbs without the intervention of visual awareness ( Milner, 2012 ; Manookin et al, 2018 ; Appleby and Manookin, 2020 ; Liu et al, 2021 ), but not for transmitting information about spatial contrast and the location of edges as required for building an internal representation of the visual scene.…”

Section: Introductionmentioning

confidence: 99%

How We See Black and White: The Role of Midget Ganglion Cells

Rezeanu

Neitz

2022

Front. Neuroanat.

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According to classical opponent color theory, hue sensations are mediated by spectrally opponent neurons that are excited by some wavelengths of light and inhibited by others, while black-and-white sensations are mediated by spectrally non-opponent neurons that respond with the same sign to all wavelengths. However, careful consideration of the morphology and physiology of spectrally opponent L vs. M midget retinal ganglion cells (RGCs) in the primate retina indicates that they are ideally suited to mediate black-and-white sensations and poorly suited to mediate color. Here we present a computational model that demonstrates how the cortex could use unsupervised learning to efficiently separate the signals from L vs. M midget RGCs into distinct signals for black and white based only correlation of activity over time. The model also reveals why it is unlikely that these same ganglion cells could simultaneously mediate our perception of red and green, and shows how, in theory, a separate small population of midget RGCs with input from S, M, and L cones would be ideally suited to mediating hue perception.

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Predictive encoding of motion begins in the primate retina

Cited by 33 publications

References 63 publications

Retinal receptive-field substructure: scaffolding for coding and computation

Retinal receptive-field substructure: scaffolding for coding and computation

Phase Advancing Is a Common Property of Multiple Neuron Classes in the Mouse Retina

How We See Black and White: The Role of Midget Ganglion Cells

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