Continuous psychophysics shows millisecond-scale visual processing delays are faithfully preserved in movement dynamics
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Summary: All three reviewers agreed that the paper lacked new biological insights. Two reviewers also raised concerns about the very low number of participants. The novelty of the task is also somewhat overstated; using tracking with different displays and varying luminance to each eye is certainly novel and enterprising, but visuomotor tracking per se is not novel, as pointed out by the reviewers.
That said, all reviewers found that the manuscript presented an interesting way to study this system, and the methods are promising given the careful and thorough recapitulation of previous results using this technique. The paper is well written, and the application of the tracking method to this specific question interesting. Reviewer #1 raised a number of subtle but not insurmountable technical issues.
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Reviewer #3:
This paper compares two methods for assessing the effect of luminance on visual processing speed. One method represents conventional methodology, using a forced choice button push approach to assess the Pulfrich effect (whereby delayed processing of horizontal motion in one eye creates a percept of motion in depth). The other, more novel method uses a continuous (monocular) tracking task to assess relative delays in signal processing caused by luminance changes. The authors show that the two approaches yield remarkably close agreement (to within a few milliseconds) in their estimates of the relative processing delays caused by luminance differences across eyes. The authors go on to establish Pulfrich-like effects in a binocular tracking task.
The paper is very clearly written, and the experiments and analyses have been …
Reviewer #3:
This paper compares two methods for assessing the effect of luminance on visual processing speed. One method represents conventional methodology, using a forced choice button push approach to assess the Pulfrich effect (whereby delayed processing of horizontal motion in one eye creates a percept of motion in depth). The other, more novel method uses a continuous (monocular) tracking task to assess relative delays in signal processing caused by luminance changes. The authors show that the two approaches yield remarkably close agreement (to within a few milliseconds) in their estimates of the relative processing delays caused by luminance differences across eyes. The authors go on to establish Pulfrich-like effects in a binocular tracking task.
The paper is very clearly written, and the experiments and analyses have been meticulously conducted. The technical quality of the work is excellent. Scientifically, the paper does not really contribute any novel insights about the nature of perceptual processing. Rather, the paper represents more of a methodological manifesto advocating for the power of tracking-based psychophysics approaches. The experiments serve as a powerful illustration of how well tracking tasks can work in practice, validated by more conventional approaches. The paper makes a compelling case that tracking tasks are able to reproduce existing findings, and can do so significantly more efficiently (i.e. in much less time).
The novelty of the approach is a bit overstated. On the first page, the authors suggest that continuous target tracking is "a new stimulus-response data collection technique". This is a bit much. People have been doing manual tracking tasks for decades, in many cases with quite sophisticated analysis and an emphasis on elucidating perceptual processing, in a similar spirit to this paper. Studies of eye movement and postural control have also employed related approaches. See, for example, the work of John Jeka, Tim Kiemel, Chris Miall, Otmar Bock, Noah Cowan - as well as the likes of Jex and McRuer in the 70s. Perhaps the authors were not aware of this substantial body of work. It seems appropriate to offer some acknowledgement and discussion of this prior work that has also recognized the power of such methods and employed them very effectively.
A significant weakness of the paper is the small number of participants who performed the tasks - only five, two of which were the authors of the paper. While the within-participant comparisons are compelling, the broader agenda of advocating for wide adoption of these tracking tasks for scientific and potentially clinical applications will need more extensive validation on much broader populations. I do share the authors' optimism about the use of tracking tasks, but broad adoption for probing perceptual processing will require demonstrations that these approaches can be robust across much larger cohorts.
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Reviewer #2:
This is a beautiful and clever paper, expanding the authors' tracking method for fast psychophysics to the domain of interocular delay. They find that it is possible to measure interocular delay quite accurately by comparing 1D tracking (in x) in each eye. The tracking technique is exciting because it potentially makes psychophysics much more accessible, and this paper demonstrates that it can be used to measure interocular timing differences.
The authors also examine whether it's possible to estimate interocular delay in a single binocular experiment where people track in depth (x and z). The answer at this point is no - while some aspects of the depth tracking are beautifully accounted for in this way, other factors clearly contribute.
I don't have any substantive concerns at all but I would be interested to see some …
Reviewer #2:
This is a beautiful and clever paper, expanding the authors' tracking method for fast psychophysics to the domain of interocular delay. They find that it is possible to measure interocular delay quite accurately by comparing 1D tracking (in x) in each eye. The tracking technique is exciting because it potentially makes psychophysics much more accessible, and this paper demonstrates that it can be used to measure interocular timing differences.
The authors also examine whether it's possible to estimate interocular delay in a single binocular experiment where people track in depth (x and z). The answer at this point is no - while some aspects of the depth tracking are beautifully accounted for in this way, other factors clearly contribute.
I don't have any substantive concerns at all but I would be interested to see some quantification of the advantage of tracking over button-press psychophysics. It's clear from the error bars in Fig 6B that button-press results are considerably more precise, but presumably they take a lot longer. Could the authors quantify this for us? E.g. button-press psychophysics: 95% confidence interval is 1ms after 100 minutes of experimentation; tracking : 95% CI is 5ms after 10 minutes, or similar.
Could you select a subset of the button-press psychophysics (fewer trials per data point) in order to say what precision could be achieved after the same time as the tracking? This would really help readers assess the costs & benefits of the two approaches.
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Reviewer #1:
This paper presents a very interesting set of techniques (monocular and binocular visuomotor tracking) to evaluate subtle differences in visual processing as a function of luminance.
Despite some technical caveats I'll explain below, the paper fairly convincing demonstrates that the monocular visuomotor tracking task can be used to identify millisecond-scale differences in visual processing lags, e.g. caused by different levels of luminance. The basic experimental analysis and comparison to traditional approaches were fairly thorough and convincing.
The binocular tracking component was less convincing, and the data were messy (which the authors acknowledge). Unfortunately, the very small sample size (N=5), lack of attention to trial order effects and learning of this new task, etc, reduce enthusiasm about this part of the …
Reviewer #1:
This paper presents a very interesting set of techniques (monocular and binocular visuomotor tracking) to evaluate subtle differences in visual processing as a function of luminance.
Despite some technical caveats I'll explain below, the paper fairly convincing demonstrates that the monocular visuomotor tracking task can be used to identify millisecond-scale differences in visual processing lags, e.g. caused by different levels of luminance. The basic experimental analysis and comparison to traditional approaches were fairly thorough and convincing.
The binocular tracking component was less convincing, and the data were messy (which the authors acknowledge). Unfortunately, the very small sample size (N=5), lack of attention to trial order effects and learning of this new task, etc, reduce enthusiasm about this part of the paper.
While this seems like a solid paper in most respects, it seems it’s primary focus is to demonstrate that a 'new' technique visuomotor tracking (which is not new per se, but may be new in this field), gives results on delay estimation that are indistinguishable from traditional psychophysical techniques. This new approach requires fewer experiments and uses the richness of the full time series for analysis. The basic approach is near and dear to my heart in that it uses continuous-time system identification to really extract rich information.
However, while I think the technique (which I quite like) is promising, I do not know what the new finding is. The analysis also only scratches the surface. I think this is a solid, field specific paper that verifies a new method and, despite its technical contributions, may be suitable for a field-specific readership, with modest effort to address or at least acknowledge the technical limitations.
Technical Limitations:
- The visuomotor behavior is not new; continuous tracking moving stimuli is an age-old process. What is potentially new here is the use of this behavior for identifying subtle differences in delay. For a fairly old review with several papers cited in this area, see:
Roth, S. Sponberg, and N. J. Cowan, "A Comparative Approach to Closed-Loop Computation," Curr Opin Neurobiol, vol. 25, pp. 54-62, 2014
But there are many (much older) papers dating back for example to McRuer on visuomotor tracking tasks for identifying control systems in human visumotor control, including careful analysis of visuomotor delay.
For a recent paper (in a non-human system) for detecting differences in delay, see:
Luminance-dependent visual processing enables moth flight in low light Sponberg et al, 2015, SCIENCE 12 JUN 2015 : 1245-1248
There are no error bars. With 40 trials per condition, a simple SEM may be sufficient.
The binocular data highlights a general problem which is that people need to learn this task, and if you are doing system identification during learning, you are doing system ID on a time varying system. This sounds like a confusing task and I agree with the authors that "higher level cognitive processes" are probably taking place but more importantly the learning system is not in steady state even after that many trials.
Very importantly, unlike the traditional psychophysics trials (which are based on perception not motor output), this data must be analyzed as a closed-loop system. There are now two pieces of visual information: exogenous reference and self-movement feedback. It is extremely likely that these are processed differently, via feedforward and feedback controllers. See these papers ... These are very new, so I wouldn't have expected the authors to know about them, but they will still be useful for understanding this concept and improving your analyses:
Yamagami, M., Howell, D., Roth, E., & Burden, S. A. (2019). Contributions of feedforward and feedback control in a manual trajectory-tracking task. IFAC-PapersOnLine, 51(34), 61-66.
Yamagami, Momona, et al. "Effect of Handedness on Learned Controllers and Sensorimotor Noise During Trajectory-Tracking." bioRxiv (2020). https://www.biorxiv.org/content/10.1101/2020.08.01.232454v1
That said, the highest-frequency responses - those picked up in the earliest moments of the impulse response function - are largely "open-loop", a fact that can be verified by noting that in the frequency domain, there is a very low gain (which is almost surely true with this data as it is in all other visuomotor tracking data across species that I am aware of, and that fundamentally must be true to ensure stable tracking!). So, the observations about short-time-scale (i.e, high frequency) differences being attributed to differences in the visual processing, are likely substantiated. But a more nuanced and accurate description of the theoretical basis for this is warranted.
- One second is not steady state in human visuomotor tasks. Tracking bandwidth for visuomotor behavior is in the ballpark of around 0.5-2Hz, which means there is still significant phase lag at 1 Hz. So the 11 second trials, with the first second thrown away does not necessarily "erase" initial conditions. As one example, see a recent paper (again I wouldn't have expected you to know this, but it still shows 1 second is not long enough):
Zimmet, A. M., Cao, D., Bastian, A. J., & Cowan, N. J. (2020). Cerebellar patients have intact feedback control that can be leveraged to improve reaching. eLife, 9, e53246.
In Fig 4S2 in that paper you see that the phase lag at 1Hz is well over 90 degrees. Always wait 10 seconds to be certain, since at 0.1Hz, the phase lag is very low.
- Perhaps most fundamentally, lag and delay are not the same thing. Delay induces a very specific time shift, but it should be noted that in a closed-loop system one can NOT just shift the closed-loop cross-correlation function (equivalent to the impulse response in this case due to the noise input). If the delay were only on the measured target signal, and not on the feedback of self-motion, then indeed a simple time shift would be adequate; but there is a complex and subtle "compounding" of the feedback delay in closed-loop that leads to a distortion, not a simple shift, of the impulse response function. These papers show different ways on how to estimate delay differences in closed loop correctly:
Luminance-dependent visual processing enables moth flight in low light Sponberg et al, 2015, SCIENCE 12 JUN 2015 : 1245-1248
Zimmet, A. M., Cao, D., Bastian, A. J., & Cowan, N. J. (2020). Cerebellar patients have intact feedback control that can be leveraged to improve reaching. eLife, 9, e53246.
I love the first paper's method, but it is not always applicable. I think it may be applicable in this case where one may be able to assume nothing changes but the delay.
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Summary: All three reviewers agreed that the paper lacked new biological insights. Two reviewers also raised concerns about the very low number of participants. The novelty of the task is also somewhat overstated; using tracking with different displays and varying luminance to each eye is certainly novel and enterprising, but visuomotor tracking per se is not novel, as pointed out by the reviewers.
That said, all reviewers found that the manuscript presented an interesting way to study this system, and the methods are promising given the careful and thorough recapitulation of previous results using this technique. The paper is well written, and the application of the tracking method to this specific question interesting. Reviewer #1 raised a number of subtle but not insurmountable technical issues.
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