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
Studying infant minds with movies is a promising way to increase engagement relative to traditional tasks. However, the spatial specificity and functional significance of movie-evoked activity in infants remains unclear. Here, we investigated what movies can reveal about the organization of the infant visual system. We collected fMRI data from 15 awake infants and toddlers aged 5–23 months who attentively watched a movie. The activity evoked by the movie reflected the functional profile of visual areas. Namely, homotopic areas from the two hemispheres responded similarly to the movie, whereas distinct areas responded dissimilarly, especially across dorsal and ventral visual cortex. Moreover, visual maps that typically require time-intensive and complicated retinotopic mapping could be predicted, albeit imprecisely, from movie-evoked activity in both data-driven analyses (i.e. independent component analysis) at the individual level and by using functional alignment into a common low-dimensional embedding to generalize across participants. These results suggest that the infant visual system is already structured to process dynamic, naturalistic information and that fine-grained cortical organization can be discovered from movie data.
