Sensitivity to image recurrence across eye-movement-like image transitions through local serial inhibition in the retina
Abstract
Standard models of stimulus encoding in the retina postulate that image presentations activate neurons according to the increase of preferred contrast inside the receptive field. During natural vision, however, images do not arrive in isolation, but follow each other rapidly, separated by sudden gaze shifts. We here report that, contrary to standard models, specific ganglion cells in mouse retina are suppressed after a rapid image transition by changes in visual patterns across the transition, but respond with a distinct spike burst when the same pattern reappears. This sensitivity to image recurrence depends on opposing effects of glycinergic and GABAergic inhibition and can be explained by a circuit of local serial inhibition. Rapid image transitions thus trigger a mode of operation that differs from the processing of simpler stimuli and allows the retina to tag particular image parts or to detect transition types that lead to recurring stimulus patterns.
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (Collaborative Research Center 889,project C1)
- Tim Gollisch
Deutsche Forschungsgemeinschaft (GO 1408/2-1)
- Tim Gollisch
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Alexander Borst, Max Planck Institute of Neurobiology, Germany
Ethics
Animal experimentation: All experimental procedures were performed in accordance with national and institutional guidelines and approved by the institutional animal care committee of the University Medical Center Goettingen (protocol number T11/35).
Version history
- Received: October 15, 2016
- Accepted: February 20, 2017
- Accepted Manuscript published: February 23, 2017 (version 1)
- Version of Record published: March 6, 2017 (version 2)
Copyright
© 2017, Krishnamoorthy et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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- Neuroscience
Probing memory of a complex visual image within a few hundred milliseconds after its disappearance reveals significantly greater fidelity of recall than if the probe is delayed by as little as a second. Classically interpreted, the former taps into a detailed but rapidly decaying visual sensory or ‘iconic’ memory (IM), while the latter relies on capacity-limited but comparatively stable visual working memory (VWM). While iconic decay and VWM capacity have been extensively studied independently, currently no single framework quantitatively accounts for the dynamics of memory fidelity over these time scales. Here, we extend a stationary neural population model of VWM with a temporal dimension, incorporating rapid sensory-driven accumulation of activity encoding each visual feature in memory, and a slower accumulation of internal error that causes memorized features to randomly drift over time. Instead of facilitating read-out from an independent sensory store, an early cue benefits recall by lifting the effective limit on VWM signal strength imposed when multiple items compete for representation, allowing memory for the cued item to be supplemented with information from the decaying sensory trace. Empirical measurements of human recall dynamics validate these predictions while excluding alternative model architectures. A key conclusion is that differences in capacity classically thought to distinguish IM and VWM are in fact contingent upon a single resource-limited WM store.
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- Neuroscience
Our ability to recall details from a remembered image depends on a single mechanism that is engaged from the very moment the image disappears from view.