doi: 10.1016/j.celrep.2021.108692.
Image luminance changes contrast sensitivity in visual cortex
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- PMID:33535047
- PMCID: PMC7886026
- DOI: 10.1016/j.celrep.2021.108692
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Image luminance changes contrast sensitivity in visual cortex
Hamed Rahimi-Nasrabadi et al. Cell Rep..
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Abstract
Accurate measures of contrast sensitivity are important for evaluating visual disease progression and for navigation safety. Previous measures suggested that cortical contrast sensitivity was constant across widely different luminance ranges experienced indoors and outdoors. Against this notion, here, we show that luminance range changes contrast sensitivity in both cat and human cortex, and the changes are different for dark and light stimuli. As luminance range increases, contrast sensitivity increases more within cortical pathways signaling lights than those signaling darks. Conversely, when the luminance range is constant, light-dark differences in contrast sensitivity remain relatively constant even if background luminance changes. We show that a Naka-Rushton function modified to include luminance range and light-dark polarity accurately replicates both the statistics of light-dark features in natural scenes and the cortical responses to multiple combinations of contrast and luminance. We conclude that differences in light-dark contrast increase with luminance range and are largest in bright environments.
Keywords: EEG; LGN; adaptation; area V1; contrast; natural scenes; primary visual cortex; receptive field; thalamocortical; thalamus.
Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.
Conflict of interest statement
Declaration of interests The authors have filed a provisional patent for the ONOFF image processing algorithm (patent application number 63127736).
Figures
(A) Natural image with low luminance range. (B) The same image with higher luminance range. (C) Cartoon illustrating how an expansion of luminance range affects the neural signaling of contrast range. (D) Stimulus combinations of contrast polarity, background luminance, and luminance range. Each rectangle represents a sequence of stimuli with different luminance contrast but the same polarity (red: light, blue: dark in all figures). The longer horizontal line on the top or the bottom of the rectangle illustrates the background luminance. The longer side of the rectangle illustrates the luminance range. (E) Stimulus temporal sequence. (F) Naka-Rushton function fit to the cortical responses and its main parameters: the luminance that generates half-maximum response (L50), the exponent (n), and the response generated by the maximum contrast (R100). L50b is L50 minus the background luminance. L50n is L50b divided by the luminance range. Lb is the stimulus luminance minus the background luminance.
(A) Top: peri-stimulus time histograms of ON responses measured in a cortical site (luminance range: 300 cd/m2, background luminance: 0 cd/m2, 30 trials per contrast). The first peak is the response to the stimulus onset (onset response) and the second the response to the stimulus turned off (rebound response). See luminance values in Method details. Bottom: onset responses (circles) fitted with a Naka-Rushton function (red line, L50b: black dotted line). The bottom right corner shows goodness of fit (R2), L50n, and non-linearity index (NL). (B and C) Same for 600 and 1,000 cd/m2 luminance range. (D–F) Same for OFF responses measured in different cortical site (background luminance: 1,000 cd/m2). For a Figure360 author presentation of this figure, seehttps://doi.org/10.1016/j.celrep.2021.108692 .
(A) Average L50b (top), L50n (center), and L50 (bottom) measured at 3 different luminance ranges from ON onset responses (n: 670, 685, and 110 cortical recording sites listed from lowest to highest luminance range). (B) Same for OFF onset responses (n: 1,113, 818, and 217 cortical recording sites listed from lowest to highest luminance range). (C) ON and OFF values superimposed for comparison. (D) Difference between OFF and ON values. *p< 0.05, p< 0.001; ns, not significant (bootstrap resampling, 50,000 repetitions). (E–H) Same for NL (top), exponent (center), and response at maximum contrast (R100, bottom). For (A)–(C), *p< 0.05, **p< 0.001; ns, not significant (2-sided Wilcoxon rank sum test). See also Figures S1 and S2.
(A) Average L50b (top) and L50 (bottom) from ON onset responses measured at different luminance backgrounds (luminance range: 300 cd/m2, n: 81, 90, 88, 85, 91, 71, 81, and 83 cortical recording sites measured at 8 different backgrounds listed from lowest to highest luminance). (B) Same for OFF onset responses (n: 146, 138, 148, 149, 145, 135, 129, and 123 cortical recording sites measured at 8 different backgrounds listed from lowest to highest luminance). (C) ON and OFF values superimposed for comparison. (D) Difference between OFF and ON values. (E–H) Same for NL (top), exponent (center), and response at maximum contrast (R100, bottom). LB: background luminance. Statistical tests and symbols as in Figure 3. See also Figure S2.
(A) Top: ON cortical responses to different stimulus contrasts measured in a human subject (luminance range: 250 cd/m2, 30 trials per contrast for each background luminance, light-dark polarity, and luminance range). Bottom: cortical responses (circles) fit with a Naka-Rushton function (line). Top left corner shows goodness of fit (R2), L50n, and NL. (B) Same for luminance range of 500 cd/m2. (C and D) Same for OFF responses. (E) OFF-ON differences in L50b measured in the same subject (white) and subject average (gray). *p< 0.05 (bootstrap resampling, 50,000 repetitions). (F) Logarithmic relation between luminance range and OFF/ON L50n ratio (bootstrap resampling, 50,000 repetitions). (G) Pupil response of same subject (top) measured at 250 (dotted line) and 500 cd/m2 luminance ranges (continuous line) at the peak (arrow) of the ON cortical response (bottom). (H) Same for OFF responses. See also Figure S3.
(A) Average luminance response functions for ON (red) and OFF (blue) cortical responses measured at 300 cd/m2 (dashed lines, n: 670 recording sites for ON, 1,113 recording sites for OFF) and 1,000 cd/m2 luminance ranges (continuous lines, n: 110 recording sites for ON, 217 recording sites for OFF). (B) Average ON and OFF image density functions of natural images with different luminance ranges (dashed lines: 0–200 cd/m2; continuous lines: 400–800 cd/m2; see sample sizes in D and E). (C) ON L50n from image density functions plotted against OFF L50n. Each dot represents an image (n: 3,061 images with median luminance >50 cd/m2). The diagonal shows the unity line. (D) Average L50b (top), L50n (center), and nonlinearity (bottom) for ON image density functions measured in natural images with different luminance ranges (n: 617, 429, and 643 images listed from lowest to highest luminance range). (E) Same for OFF image density functions (n: 2,227, 534, and 253 images listed from lowest to highest luminance range). (F) Superimposed ON and OFF values. (G) Difference between OFF and ON values. (H) Normalized bootstrap histograms of OFF/ON L50n log ratios from natural images (left), cat visual cortex (center), and human visual cortex (right). High/low range: ratio of luminance range. Adaptation slope: logarithm of OFF/ON L50n ratio divided by the logarithm of the high/low range (bootstrap resampling, n: 50,000 repetitions). Statistical tests and symbols as in Figure 3.
(A) The left panels show a natural image (van Hateren and van der Schaaf, 1998) normalized by its maximum (top) and a histogram of image pixel intensity (bottom, 1,024 × 1,531 pixels). The other panels show the same for images processed with IMADJUST, CLAHE, and ON-OFF algorithms. (B) Contrast gain from IMADJUST (black), CLAHE (green), and ON-OFF (blue, n: 4,167 images). (C) Correlations between the mean luminance of the original image and the pixel intensity of the processed image (n: 4,167 images). (D) ON and OFF L50 (x axis) can be accurately predicted (y axis) with linear regression models (equations at the top) for both onset responses (left) and rebound responses (right). Notice that for each combination of background and range, the model returns a single value, but the measured L50 is more variable (n: 331 recording sites for ON onset responses, 520 recording sites for OFF onset responses, 275 recording sites for ON rebound responses, and 321 for OFF rebound responses). (E) Left: ON and OFF L50 of the image density functions (x axis) and prediction (y axis) with a linear model (equations at the top, n: 3,247 ON images and 3,247 OFF images with mean luminance >50 cd/m2). Right: same as left but for the exponent of the ON and OFF functions (n: 3,112 ON images and 3,175 OFF images with accurately fitted luminance response functions, R2 > 0.9). (F) Correlations of the image L50n with the skewness (left) and kurtosis (center) of the luminance distributions, and model predictions (right, equations at the top, n: 3,247 ON images and 3,247 OFF images with mean luminance >50 cd/m2). (G) Definition of ONOFF contrast. DVC, dark visual contrast; LVC, light visual contrast; Range, luminance range; Sb, stimulus luminance minus background luminance. See also Figure S4.
Comment in
- Darks and Lights, the 'Yin-Yang' of Vision Depends on Luminance.Jancke D.Jancke D.Trends Neurosci. 2021 May;44(5):339-341. doi: 10.1016/j.tins.2021.02.007. Epub 2021 Mar 9.Trends Neurosci. 2021.PMID:33712269
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