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Backward masking in mice requires visual cortex

Nature Neuroscience volume 27, pages 129–136 (2024)Cite this article

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Abstract

Visual masking can reveal the timescale of perception, but the underlying circuit mechanisms are not understood. Here we describe a backward masking task in mice and humans in which the location of a stimulus is potently masked. Humans report reduced subjective visibility that tracks behavioral deficits. In mice, both masking and optogenetic silencing of visual cortex (V1) reduce performance over a similar timecourse but have distinct effects on response rates and accuracy. Activity in V1 is consistent with masked behavior when quantified over long, but not short, time windows. A dual accumulator model recapitulates both mouse and human behavior. The model and subjects’ performance imply that the initial spikes in V1 can trigger a correct response, but subsequent V1 activity degrades performance. Supporting this hypothesis, optogenetically suppressing mask-evoked activity in V1 fully restores accurate behavior. Together, these results demonstrate that mice, like humans, are susceptible to masking and that target and mask information is first confounded downstream of V1.

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Fig. 1: Backward visual masking impairs discrimination of target location.
Fig. 2: Visual cortical activity during a 50-ms window is required for target detection.
Fig. 3: A dual accumulator model using V1 activity is consistent with the performance and reaction times of mice.
Fig. 4: Optogenetic inhibition of mask-evoked activity in visual cortex rescues accuracy of behavioral responses.

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Data availability

Data is deposited on figshare at https://doi.org/10.6084/m9.figshare.24135018.v1.

Code availability

Code is available on GitHub at https://github.com/samgale/Masking.

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Acknowledgements

We thank the Allen Institute founder, P. G. Allen, for his vision, encouragement and support. We thank the Allen Institute Neurosurgery and Behavior team for help with mouse surgeries. We thank S. Naylor for support with program management. We thank S. Reynolds for help with administration of the animal and human protocols. We thank M. Watanabe and D. Ollerenshaw for discussion of masking paradigms in rodents. We thank the Tiny Blue Dot Foundation for providing funding for this study. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the paper.

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Authors and Affiliations

  1. MindScope Program, Allen Institute, Seattle, WA, USA

    Samuel D. Gale, Chelsea Strawder, Corbett Bennett, Stefan Mihalas, Christof Koch & Shawn R. Olsen

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  1. Samuel D. Gale
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Contributions

S.D.G., C.B., C.K. and S.R.O. conceived the project. S.D.G., C.S., C.B. and S.R.O. developed the mouse and human experimental methodology. S.D.G. and C.S. performed the experiments. S.D.G. and C.B. analyzed the data. S.M. provided advice on modeling and data analysis. C.K. and S.R.O. supervised all aspects of the project. All authors contributed to writing the paper.

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Correspondence to Christof Koch or Shawn R. Olsen.

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Competing interests

C.K. holds an executive position, and has financial interest, in Intrinsic Powers, Inc., a company whose purpose is to develop a device that can be used in the clinic to assess the presence and absence of consciousness in patients. This does not pose any conflict of interest with regard to the work undertaken for this publication.

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Extended data

Extended Data Fig. 1 Sensitivity of task performance in mice to target duration and contrast in the absence of a mask.

Sensitivity of task performance in mice to target duration (a-c) and contrast (d-f) in the absence of a mask. Target contrast was 100% for experiments varying target duration (A-C). Target duration was 17 ms for experiments varying target contrast (D-F). Colored lines are data from single sessions from individual mice (n = 8 wild-type mice, 10 VGAT-ChR2 mice). Black circles are means across mice; error bars represent standard error of the mean.

Extended Data Fig. 2 Statistical comparisons of performance across conditions shown in Fig. 1.

(a,b) p-values from comparison of mouse response rates (A) and accuracy (B) for the conditions shown in Fig. 1b,c. Distributions were compared with a Kruskal-Wallis test followed by pairwise Wilcoxon rank sum tests. p-values were corrected for multiple comparisons using the Benjamini-Hochberg method. Greyness scale is log10 based. Significant p-values (<0.05) are marked by red stars. Non-significant p-values (≥0.05) are white. Redundant or non-tested comparisons are yellow. (c-e) Same as A and B for human subjects (Fig. 1d–f), additionally showing comparisons of subjective visibility ratings (E).

Extended Data Fig. 3 Selection of units and timing of visual responses.

(a) False-positive rate for spikes recorded from 1382 units from 5 wild-type and 4 VGAT-ChR2 mice. The false-positive rate was defined as the refractory-period violation rate (number of spikes within 1.5 ms refractory periods divided by the total duration of refractory periods) divided by the total spike rate (see Methods). Units with a false-positive rate greater than one by this definition are displayed at one in the histogram. 543 units with false-positive rates less than 0.5 were considered for further analysis in this study. (b) Peak-to-trough duration of the average spike waveforms (n = 543). Units with peak-to-trough duration less than 0.4 were classified as fast spiking (FS; putative inhibitory interneurons); all other units were classified as regular spiking (RS; putative pyramidal neurons). (c) Average firing rate of 173 visually responsive units (see Methods) following presentation of a contralateral target (17 ms duration) or bilateral mask (200 ms duration) starting at 0 ms on the x-axis. Shaded area is the standard error of the mean. (d) Cumulative distribution of the median time to first spike (see Methods) of the 173 visually responsive units. There was no significant difference in the time to first spike between target-only (median across units 73.9 ms) and mask-only (71.3 ms) trials (p = 0.22, Wilcoxon rank sum test). There was also no significant difference between the time to first spike of RS (n = 128) and FS (n = 45) units (target only: 75.1 vs. 68.1 ms, p = 0.08; mask only: 71.4 vs. 68.9 ms, p = 0.39), which were combined for the data plotted.

Extended Data Fig. 4 Effect of optogenetic stimulus in V1 neurons in VGAT-ChR2 mice.

(a) Mean response of V1 neurons from 4 VGAT-ChR2 mice to stimulation with blue light. Gray, shaded region indicates standard error of the mean. Fast-spiking (FS, putative interneurons) and regular spiking (RS, putative pyramidal neurons) were defined by the peak-to-trough duration of their spike waveforms. Neurons were classified as excited, transiently excited, or inhibited (see Methods). Two neurons were non-responsive (not shown). The bottom panel expands the time scale (indicated by dashed lines) of the inhibited cells. (b) Mean response of 74 visually-responsive V1 neurons (see Methods) from the same mice in A to the visual and optogenetic stimuli used for the behavior data in Fig. 4a,b. Shaded regions indicate standard error of the mean. Neurons that were excited or transiently excited by the optogenetic light were excluded. Optogenetic light onset was varied relative to the onset of the target presented contralateral or ipsilateral to the recorded neurons. On a subset of trials, the target (17 ms duration) was immediately followed by a bilateral mask for 200 ms.

Extended Data Fig. 5 Statistical comparison of performance accross conditions shown in Fig. 2, effect of unilateral cortical inhibition, and control experiment in wildtype mice.

(a,b) p-values from comparison of response rates (A) and accuracy (B) for the conditions shown in Fig. 2c,d, using statistical procedures described in the legend for Extended Data Fig. 2a,b. (c) Effect of unilateral cortical inhibition on target detection (n = 8 VGAT-ChR2 mice). The inhibited hemisphere(s) are indicated on the x-axis. Optogenetic light onset was 17 ms before target onset. The top plot shows, for trials on which the target was left, the mean fraction of trials that mice moved right (red, correct) or left (blue, incorrect). Error bars represent the standard error the mean. The sum of the red and blue data points for each condition is the response rate. The middle and bottom plots show similar data for target-right and no visual stimulus trials, respectively. (d,e) Effect of optogenetic light stimulus on response rate and accuracy in wild-type mice (n = 8) for the same conditions shown in Fig. 2c,d. Circles are means across mice; error bars represent standard error of the mean.

Extended Data Fig. 6 Cumulative spikes relative to stimulus onset for contralateral or ipsilateral stimuli.

(a) Cumulative stimulus-evoked spikes over 200 ms per V1 neuron (n = 58) following onset of a contralateral target. Spike number was calculated by integrating the trial-averaged post-stimulus time histogram after baseline subtraction for each neuron, and then averaging across neurons. Shaded region surrounding each line represents the standard error of the mean in A-C. (b) Same as A for trials with an ipsilateral target. (c) The average difference of the values quantified in A and B (see also Fig. 3b,c).

Extended Data Fig. 7 Additional reaction time and movement speed data and modeling of human data.

(a) Median reaction times for all responses, correct responses, and incorrect responses from the 16 mice used for Fig. 1b,c. Circles are means across mice and error bars represent standard error of the mean. (b) Comparison of median reaction times for correct and incorrect responses for each mouse. Each circle is data for one condition (mask onset or target only) from one mouse. (c) Cumulative probability distributions of reaction times pooled across the mice for correct (solid lines) and incorrect (dashed lines) responses. Reaction times on mask-only and catch trials are also shown. (d,e) Same as B,C for movement speed. (f-h) Same as A-C for the reaction times of 16 human subjects. (i) Fraction correct versus reaction time after pooling reaction times across all humans in 600 ms bins. Shaded region surrounding each line is the 95% confidence interval given the fraction correct values and the number of pooled trials for each bin (the median number of trials across mask onset conditions was 135, 296, 30, and 28 for the time bins from left to right after excluding conditions from a bin if there were less than 15 trials). (j-l) Response rate, accuracy, and reaction times of the dual accumulator model (open circles) shown in Fig. 3f fit to human behavior data (filled circles with error bars representing the standard error of the mean from 16 humans). (m) Accuracy versus reaction time for the model, corresponding to I for humans.

Extended Data Fig. 8 Statistical comparison of performance across conditions shown in Fig. 4 and control experiment in wild-type mice.

(a,b) p-values from comparison of response rates (A) and accuracy (B) for the conditions shown in Fig. 4a,b, using statistical procedures described in the legend for Extended Data Fig. 2a,b. (c,d) Effect of optogenetic light stimulus on response rate and accuracy in wild-type mice (n = 8) for the same conditions shown in Fig. 4a,b. Circles are means across mice; error bars represent standard error of the mean.

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Gale, S.D., Strawder, C., Bennett, C. et al. Backward masking in mice requires visual cortex. Nat Neurosci 27, 129–136 (2024). https://doi.org/10.1038/s41593-023-01488-0

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