Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina

  1. Maxwell H Turner  Is a corresponding author
  2. Gregory W Schwartz
  3. Fred Rieke
  1. University of Washington, United States
  2. Northwestern University, United States
8 figures and 2 additional files

Figures

Circuit basis of the surround and implications for receptive field (RF) structure.

(A,B) Two models for how the surround is integrated with the center to form the full RF: The linear-nonlinear model shown in (A) linearly combines the center and surround before treatment with an …

https://doi.org/10.7554/eLife.38841.002
Figure 2 with 1 supplement
The RF surround regulates nonlinear spatial integration of natural images.

(A) We presented a natural image patch and its linear-equivalent disc stimulus to probe sensitivity to spatial contrast in natural scenes. Rows of each raster correspond to repeated presentations of …

https://doi.org/10.7554/eLife.38841.003
Figure 2—source data 1

Included is a .mat file containing a data structure for the data in Figure 2.

Individual trial responses are included as binary vectors of spike times for natural image and associated linear equivalent disc stimuli, across a range of surround contrast conditions. Data are organized by cell and then by natural image. The natural image used in each set of responses is also included. For all responses, data are sampled at 10 Khz, and both center and surround stimuli appear after 200 ms and persist for 200 ms.

https://doi.org/10.7554/eLife.38841.005
Figure 2—figure supplement 1
Measuring linear center-surround structure in parasol RGCs.

(A) Off parasol RGC spike responses to expanding spots stimuli. (B) Area-summation curve from the cell in (A), points show mean ± S.E.M., smooth curve is a difference-of-Gaussians fit. (C–D) Same …

https://doi.org/10.7554/eLife.38841.004
Figure 3 with 1 supplement
The RF surround regulates nonlinear spatial integration in the RF center.

(A) Left column: Example Off parasol RGC spike response to an isolated split-field grating stimulus in the RF center. Rows of each raster correspond to repeated presentations of the same stimulus …

https://doi.org/10.7554/eLife.38841.006
Figure 3—source data 1

Included is a .mat file containing a data structure for the data in Figure 3A–C.

Off parasol RGC spike responses are included as raw traces and binary vectors of spike times for a range of central grating contrasts and surround contrasts. For all responses, data are sampled at 10 Khz, and both center and surround stimuli appear after 200 ms and persist for 200 ms.

https://doi.org/10.7554/eLife.38841.008
Figure 3—source data 2

Included is a .mat file containing a data structure for the data in Figure 3D–F.

Off parasol RGC excitatory current responses (in units of pA) have been baseline-subtracted. For all responses, data are sampled at 10 Khz, and both center and surround stimuli appear after 200 ms and persist for 200 ms.

https://doi.org/10.7554/eLife.38841.009
Figure 3—source data 3

Included is a .mat file containing a data structure for the data in Figure 3—figure supplement 1.

On parasol RGC excitatory current responses (in units of pA) and have been baseline-subtracted. For all responses, data are sampled at 10 Khz, and both center and surround stimuli appear after 200 msec and persist for 200 ms.

https://doi.org/10.7554/eLife.38841.010
Figure 3—figure supplement 1
Regulation of spatial integration by the RF surround of On parasol RGCs.

Compare to Figure 3A–C. (A) Left: On parasol RGC excitatory current response to a split-field grating stimulus in the RF center. Right: when the center stimulus is paired with a dark surround …

https://doi.org/10.7554/eLife.38841.007
Figure 4 with 1 supplement
Linear-nonlinear cascade modeling supports an architecture where center and surround combine linearly before passing through a shared nonlinearity.

(A) We presented Gaussian noise to either the center region (left), surround region (middle) or center and surround regions simultaneously (right) while measuring excitatory synaptic current …

https://doi.org/10.7554/eLife.38841.011
Figure 4—source data 1

Included is a .mat file containing a data structure for the data in Figure 4 and 5.

Stimuli and corresponding responses of On and Off parasol RGCs to center-surround white noise stimulation have been concatenated into vector arrays. Note that the data were collected in interleaved trials. This data includes excitatory conductance responses (in nS) that were estimated using measured excitatory current responses and an estimate of the excitatory driving force for each cell. Data are sampled at 10 Khz.

https://doi.org/10.7554/eLife.38841.013
Figure 4—figure supplement 1
Representative predictions of linear-nonlinear cascade models for center-surround interactions.

Representative traces for the center-surround LN cascade models fit to the example cell in Figure 4. Top: center-surround stimulus trace; middle: associated generator signal for the center and …

https://doi.org/10.7554/eLife.38841.012
The RF surround changes the apparent rectification of inputs from the center.

(A) Response surface showing the mean excitatory conductance response from an Off parasol RGC as a function of filtered inputs to both the center and surround (center or surround ‘activation’, that i…

https://doi.org/10.7554/eLife.38841.014
Natural movie stimuli elicit nonlinear interactions between the RF center and surround.

(A) Natural image and associated eye movement trajectory from (Van Der Linde et al., 2009). Right: example movie frames showing isolated center (top), surround (middle), and center-surround stimuli …

https://doi.org/10.7554/eLife.38841.015
Spatial correlations in natural scenes promote nonlinear center-surround interactions.

(A) Example image (van Hateren and van der Schaaf, 1998) used to construct natural intensity stimuli. (B) Intensity histogram from the image in (A). Dashed vertical line indicates the mean …

https://doi.org/10.7554/eLife.38841.016
Figure 7—source data 1

Included is a .mat file containing a data structure for the data in Figure 7A–G.

The structure contains excitatory current responses (baseline subtracted, in pA) of On and Off parasol RGCs to center-surround naturalistic luminance stimuli. Data are sampled at 10 Khz.

https://doi.org/10.7554/eLife.38841.017
Figure 8 with 2 supplements
Intensity correlations across space promote nonlinear spatial integration in the RF center.

(A) Schematic showing the hypothesized interaction between center and surround inputs on local subunit rectification. A depolarizing input to the center may push the synapse into a locally linear …

https://doi.org/10.7554/eLife.38841.018
Figure 8—figure supplement 1
Center-surround intensity differences modulate spatial contrast sensitivity for randomly shuffled natural surrounds.

From the data shown in Figure 8D–F using the shuffled surround condition, we plotted thenonlinearity index as a function of the difference in mean intensity between the RF center and surround. …

https://doi.org/10.7554/eLife.38841.019
Figure 8—figure supplement 2
A spatiotemporal RF model also shows modulation of spatial contrast sensitivity with surround activation.

Compare to Figure 8G–I, which shows results for a simpler, spatial-only RF model. (A) In addition to the spatial subunit filters, this spatiotemporal model includes temporal linear filters which …

https://doi.org/10.7554/eLife.38841.020

Additional files

Source code 1

Example MATLAB code to load the Source Data files, plot responses, and perform basic analyses.

The analysis used to generate the figures in the paper is included in the corresponding GitHub repository (see Materials and methods) – this Source Code file is merely illustrative of how to access and interact with the provided Source Data files.

https://doi.org/10.7554/eLife.38841.021
Transparent reporting form
https://doi.org/10.7554/eLife.38841.022

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