Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina
- University of Washington, United States
- Northwestern University, United States
Abstract
Antagonistic receptive field surrounds are a near-universal property of early sensory processing. A key assumption in many models for retinal ganglion cell encoding is that receptive field surrounds are added only to the fully formed center signal. But anatomical and functional observations indicate that surrounds are added before the summation of signals across receptive field subunits that creates the center. Here, we show that in the macaque monkey retina this receptive field architecture has an important consequence for spatial contrast encoding: the surround can control sensitivity to fine spatial structure by changing the way the center integrates visual information over space. The impact of the surround is particularly prominent when center and surround signals are correlated, as they are in natural stimuli. This effect of the surround differs substantially from classic center-surround models and raises the possibility that the surround plays unappreciated roles in shaping ganglion cell sensitivity to natural inputs.
Data availability
We have made all the data in the study freely available. Source data files have been provided for Figures 2, 3, 4 and 7, and example code to demonstrate how to pull out and plot the data is provided as Source code file 1.
Article and author information
Author details
Funding
National Eye Institute (F31-EY026288)
- Maxwell H Turner
National Eye Institute (EY11850)
- Fred Rieke
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: Tissue was obtained via the tissue distribution program at the Washington National Primate Research Center. All animal procedures were performed in accordance with IACUC protocols at the University of Washington (IACUC protocol number 4277-01).
Copyright
© 2018, Turner 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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Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina
eLife 7:e38841.
https://doi.org/10.7554/eLife.38841
Further reading
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- Neuroscience
The infralimbic cortex (IL) is essential for flexible behavioral responses to threatening environmental events. Reactive behaviors such as freezing or flight are adaptive in some contexts, but in others a strategic avoidance behavior may be more advantageous. IL has been implicated in avoidance, but the contribution of distinct IL neural subtypes with differing molecular identities and wiring patterns is poorly understood. Here, we study IL parvalbumin (PV) interneurons in mice as they engage in active avoidance behavior, a behavior in which mice must suppress freezing in order to move to safety. We find that activity in inhibitory PV neurons increases during movement to avoid the shock in this behavioral paradigm, and that PV activity during movement emerges after mice have experienced a single shock, prior to learning avoidance. PV neural activity does not change during movement toward cued rewards or during general locomotion in the open field, behavioral paradigms where freezing does not need to be suppressed to enable movement. Optogenetic suppression of PV neurons increases the duration of freezing and delays the onset of avoidance behavior, but does not affect movement toward rewards or general locomotion. These data provide evidence that IL PV neurons support strategic avoidance behavior by suppressing freezing.
