The pupillary light response as a physiological index of aphantasia, sensory and phenomenological imagery strength

  1. Lachlan Kay
  2. Rebecca Keogh
  3. Thomas Andrillon
  4. Joel Pearson

  • Curated by eLife

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    Evaluation Summary:

    This is an interesting study of the relation between vividness of visual imagery and the pupillary light response that can result from it. It provides evidence for the absence of imagery in individuals that self-report as aphantasic. The results will likely be of interest to researchers in a range of disciplines such as psychology, neuroscience and philosophy. There were some shared concerns related to demand characteristics and eye movements, and the authors might be able to address these concerns with more data analysis and/or control experiments.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.”)

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Abstract

The pupillary light response is an important automatic physiological response which optimizes light reaching the retina. Recent work has shown that the pupil also adjusts in response to illusory brightness and a range of cognitive functions, however, it remains unclear what exactly drives these endogenous changes. Here, we show that the imagery pupillary light response correlates with objective measures of sensory imagery strength. Further, the trial-by-trial phenomenological vividness of visual imagery is tracked by the imagery pupillary light response. We also demonstrated that a group of individuals without visual imagery (aphantasia) do not show any significant evidence of an imagery pupillary light response, however they do show perceptual pupil light responses and pupil dilation with larger cognitive load. Our results provide evidence that the pupillary light response indexes the sensory strength of visual imagery. This work also provides the first physiological validation of aphantasia.

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  1. Version published to 10.7554/elife.72484 on eLife
  2. eLife

    Author Response:

    First we would like to thank the reviewers for their very kind words regarding our manuscript and for their helpful suggestions for how to improve our paper. We believe their suggestions have helped to strength the paper as a whole. We will address below the specific weaknesses that the reviewers have brought up and describe how we have modified our manuscript in response to these suggestions.

    Reviewer #1:

    This is an interesting study of the relation between vividness of visual imagery and the pupillary light response that can result from it. The authors collected data in two experimental paradigms, which they ran in two independent samples. One of these samples was a larger group of psychology students; the other a self-reported group of people with aphantasia. In a first paradigm, the authors show that a lack of vivid imagery is associated with a smaller (or even absent) pupillary light response. Using a second paradigm, binocular rivalry, they show that the degree to which imagery primes binocular rivalry is correlated (to a degree that is quite striking) with the magnitude of the pupillary light response to imagined stimuli. These results were obtained both for low-scoring individuals in the large sample as well as for the aphantasics. The study provides objective evidence for the absence of imagery in individuals that self-report as aphantasic.

    The paper is well written and all the necessary controls for potentially confounding variables are in place. For instance, age or visual persistence are discussed and excluded as alternative explanations based on convincing analyses. A particular strength of the manuscript is that the authors report positive results for pupillary responses in the group with aphantasia. That is, these individuals show regular pupillary responses to changes in physical stimulus brightness as well as to cognitive load. Another strength is that the group of aphantasics was invited separately and not determined post-hoc in the initial sample.

    In summary, there is a lot to like about this paper. I have three comments / questions that I think should be addressed, however.

    1. A point that I would like to see analyzed and discussed is the role of eye movements. The authors do not report any analyses of fixation behavior or the frequency of saccades in the two groups. These should be analyzed and reported. The only mention of fixation control is in lines 423-424, but the authors remain at a very superficial level, stating that footage from this scene camera of the pupil labs eye tracker was "assessed to ensure fixation on the computer monitor". Does this mean that participants could look anywhere provided they looked at the monitor?

    We have now analysed the eye-movements of participants to assess whether or not they might be driving some of our findings, which we agree is a very important additional analysis to add to this paper to confirm our findings are not being driven by eye-movements. When analysing both eccentricity and the number of saccades participants made there was no differences between the two groups when imagining the triangles (see supplementary figures s7 and s11). There was also no correlation between eccentricity data and either the imagery pupillary light reflex or binocular rivalry priming. Taken together it seems unlikely that the observed pupillary light response during imagery is being driven by eye-movements.

    1. In Figure 1D (also lines 120-124), the authors show a correlation between vividness ratings and the pupillary light response. I assume that participants differ substantially in their distributions of responses. So these correlations could be a consequence of individual differences or they could provide evidence for trial-by-trial variation. There might be ways to find out. For instance, is there evidence for these correlations at the level of individuals? Does the correlation persist if individual vividness-response distributions are normalized to span the same range for each observer?

    We would like to clarify the analysis we ran. Figure 1D is the results of 2 x 4 linear mixed-effects analysis, not correlations. This model included subject identity as a random effect (see Methods section of our paper) and therefore the effects reported were computed at the subject level. We report in the text, effects that are significant at the level of the sample. This does not exclude the possibility of inter-individual differences, but we are not sure how interpretable a single-subject analysis is in the current study.

    1. In lines 314-315, the authors state that the pupillary light response to imagined stimuli may serve as an objective indicator of aphantasia. I think this is taking the interpretation of the data too far, mainly for two reasons. First, the authors haven't shown that low pupillary light response predicts aphantasia in a group of people that does not self-report as aphantasics before the test. Second, the absence of a pupillary light response (in a new sample with no additional controls) could also indicate a lack of motivation to engage in imagery. The authors should thus clarify that such tests would always have to be combined with positive tests that show the commitment of participants to the task instructions.

    We agree that it is very important to include positive controls in not only pupillary light response imagery tasks, but any task that measures imagery or any other internal experience. We have now expanded on this point in our discussion as well as reporting on the mock binocular rivalry trials that were included in the priming imagery task as a control for potential response biases.

    Reviewer #2:

    Kay et al. investigated visual mental imagery in the general population and the lack thereof in individuals with aphantasia by measuring the pupillary light response to imagined light and dark shapes. Their findings are twofold. First, they show a link between pupil size change and perceived vividness of imagery and corroborate this finding using another established objective measure of vividness. Secondly, they found a lack of such a pupillary light response in a group of individuals who maintain no visual experience of imagery. This demonstrates the usefulness of using the pupillary light response as a measure of subjective vividness of imagery and potentially demonstrates the first physiological finding in aphantasia.

    Strengths

    The experiment incorporates several different dimensions into a single clean design that is useful for isolating and tracking multiple relevant measures. First, by having the brightness of the perceived and imagined shapes vary across trials, the authors could show that changes in the pupillary light response correspond to changes in imagined brightness. The authors also added in an independent number-of-objects dimension since pupil size also varies with cognitive effort. This provided evidence that aphantasic subjects were attempting to imagine, since the pupil size did change with set size, even when it didn't change with brightness. Finally, by having subjects report the perceived vividness of each imagined image, the authors could link subjective experience of imagery to the pupillary light response.

    The authors also strengthen their findings by comparing changes in pupil size to an objective measure of imagery vividness. By leveraging the fact that imagery mimics vision's ability to bias a perception during binocular rivalry, the authors avoid the severe limitations present in measures that rely on introspection only.

    Weaknesses

    Due to the inherently private nature of mental imagery, ruling out fabrication or demand characteristics is extremely difficult. This is especially true in aphantasia research, as we are often looking for the absence of an effect rather than an enhancement. Readers should keep in mind that, while the authors made some effort to confirm that the aphantasic subjects were attempting to imagine, the potential for this and other biases were not ruled out. Without the use of probes to test subjects on the remembered/imagined objects and reporting the outcomes of catch trials, it is difficult to tell whether subjects were fully engaging with the stimuli.

    Readers should also take the pupillary light response as a tool to add to the battery of assessments for aphantasia, not as one that a diagnosis can be based on alone. While the authors do show a group level difference in pupil size in response to imagined shapes and claim it as a "new low-cost objective measure for aphantasia", it should be remembered that this manuscript does not demonstrate the tool's efficacy in identifying individual subjects with aphantasia. The absence/presence of an imagery pupillary light response does not confirm/rule out aphantasia.

    Overall, the manuscript helps characterize an intriguing condition that until relatively recently received little empirical attention. These findings support the internal experiences described by aphantasic individuals, experiences that are often met with skepticism. Importantly, the authors have also offered the field a new objective physiological approximation of imagery vividness which can be incorporated into a number of study designs examining changes in imagery. The majority of previous measures relied on self-report alone and often suffered from the limitations of language (e.g., what it means for something to be "like vision" can be very different for different people). This manuscript also adds to the growing body of evidence of the power of internally generated signals, which can apparently reach all the way down the visual hierarchy to the eyes themselves.

    We are in full agreement that when we investigate the internal contents of the mind we need to be mindful of the many caveats that exist when relying on people’s ability to introspect. We agree that future studies should expand on our research by adding in further controls, such as having participants report what item they were asked to remember at the end of the trial. However researchers should also keep in mind that changing the demands of a task can alter how participants undertake a given task. For example by emphasising remembering the items, rather than creating detailed vivid images in mind, participants may revert to a non-visual imagery strategy to remember the items, such as labelling the items. This may be particularly easy to do in the current study as the items being imagined are simple geometric shapes. Indeed it was important to avoid this potential pitfall here with our aphantasic population as we have previously shown that aphantasic individuals can perform a wide array of visual working memory tasks despite their lack of visual imagery. We believe that the addition of a set-size/cognitive load condition, plus our added reporting on mock trails helps to answer some of these potential response bias issues, but future research can and should further investigate these potential biases in greater detail.

    The second point Reviewer #2 brings up is a very good one, that no one singular measure in isolation, at this point in time, can be used to ‘diagnose’ aphantasia. The field is very young and we are still in the process of understanding exactly what aphantasia is. For example there may be many subtypes of aphantasia, with previous work from our group and others showing that aphantasic individuals are heterogenous in their reporting of how other imagery modalities are affected. We agree with Reviewer #2’s point that a battery of tests, potentially comprising questionnaires (e.g. VVIQ), psychophysical tasks (e.g. binocular rivalry paradigm) and physiological (e.g. skin conductance, pupillometry) should be aimed for where possible in testing aphantasic populations. The pupillary light response is a new tool that can be added to this arsenal.

  3. eLife

    Evaluation Summary:

    This is an interesting study of the relation between vividness of visual imagery and the pupillary light response that can result from it. It provides evidence for the absence of imagery in individuals that self-report as aphantasic. The results will likely be of interest to researchers in a range of disciplines such as psychology, neuroscience and philosophy. There were some shared concerns related to demand characteristics and eye movements, and the authors might be able to address these concerns with more data analysis and/or control experiments.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.”)

  4. eLife

    Reviewer #1 (Public Review):

    This is an interesting study of the relation between vividness of visual imagery and the pupillary light response that can result from it. The authors collected data in two experimental paradigms, which they ran in two independent samples. One of these samples was a larger group of psychology students; the other a self-reported group of people with aphantasia. In a first paradigm, the authors show that a lack of vivid imagery is associated with a smaller (or even absent) pupillary light response. Using a second paradigm, binocular rivalry, they show that the degree to which imagery primes binocular rivalry is correlated (to a degree that is quite striking) with the magnitude of the pupillary light response to imagined stimuli. These results were obtained both for low-scoring individuals in the large sample as well as for the aphantasics. The study provides objective evidence for the absence of imagery in individuals that self-report as aphantasic.

    The paper is well written and all the necessary controls for potentially confounding variables are in place. For instance, age or visual persistence are discussed and excluded as alternative explanations based on convincing analyses. A particular strength of the manuscript is that the authors report positive results for pupillary responses in the group with aphantasia. That is, these individuals show regular pupillary responses to changes in physical stimulus brightness as well as to cognitive load. Another strength is that the group of aphantasics was invited separately and not determined post-hoc in the initial sample.

    In summary, there is a lot to like about this paper. I have three comments / questions that I think should be addressed, however.

    1. A point that I would like to see analyzed and discussed is the role of eye movements. The authors do not report any analyses of fixation behavior or the frequency of saccades in the two groups. These should be analyzed and reported. The only mention of fixation control is in lines 423-424, but the authors remain at a very superficial level, stating that footage from this scene camera of the pupil labs eye tracker was "assessed to ensure fixation on the computer monitor". Does this mean that participants could look anywhere provided they looked at the monitor?

    2. In Figure 1D (also lines 120-124), the authors show a correlation between vividness ratings and the pupillary light response. I assume that participants differ substantially in their distributions of responses. So these correlations could be a consequence of individual differences or they could provide evidence for trial-by-trial variation. There might be ways to find out. For instance, is there evidence for these correlations at the level of individuals? Does the correlation persist if individual vividness-response distributions are normalized to span the same range for each observer?

    3. In lines 314-315, the authors state that the pupillary light response to imagined stimuli may serve as an objective indicator of aphantasia. I think this is taking the interpretation of the data too far, mainly for two reasons. First, the authors haven't shown that low pupillary light response predicts aphantasia in a group of people that does not self-report as aphantasics before the test. Second, the absence of a pupillary light response (in a new sample with no additional controls) could also indicate a lack of motivation to engage in imagery. The authors should thus clarify that such tests would always have to be combined with positive tests that show the commitment of participants to the task instructions.

  5. eLife

    Reviewer #2 (Public Review):

    Kay et al. investigated visual mental imagery in the general population and the lack thereof in individuals with aphantasia by measuring the pupillary light response to imagined light and dark shapes. Their findings are twofold. First, they show a link between pupil size change and perceived vividness of imagery and corroborate this finding using another established objective measure of vividness. Secondly, they found a lack of such a pupillary light response in a group of individuals who maintain no visual experience of imagery. This demonstrates the usefulness of using the pupillary light response as a measure of subjective vividness of imagery and potentially demonstrates the first physiological finding in aphantasia.

    Strengths

    The experiment incorporates several different dimensions into a single clean design that is useful for isolating and tracking multiple relevant measures. First, by having the brightness of the perceived and imagined shapes vary across trials, the authors could show that changes in the pupillary light response correspond to changes in imagined brightness. The authors also added in an independent number-of-objects dimension since pupil size also varies with cognitive effort. This provided evidence that aphantasic subjects were attempting to imagine, since the pupil size did change with set size, even when it didn't change with brightness. Finally, by having subjects report the perceived vividness of each imagined image, the authors could link subjective experience of imagery to the pupillary light response.

    The authors also strengthen their findings by comparing changes in pupil size to an objective measure of imagery vividness. By leveraging the fact that imagery mimics vision's ability to bias a perception during binocular rivalry, the authors avoid the severe limitations present in measures that rely on introspection only.

    Weaknesses

    Due to the inherently private nature of mental imagery, ruling out fabrication or demand characteristics is extremely difficult. This is especially true in aphantasia research, as we are often looking for the absence of an effect rather than an enhancement. Readers should keep in mind that, while the authors made some effort to confirm that the aphantasic subjects were attempting to imagine, the potential for this and other biases were not ruled out. Without the use of probes to test subjects on the remembered/imagined objects and reporting the outcomes of catch trials, it is difficult to tell whether subjects were fully engaging with the stimuli.

    Readers should also take the pupillary light response as a tool to add to the battery of assessments for aphantasia, not as one that a diagnosis can be based on alone. While the authors do show a group level difference in pupil size in response to imagined shapes and claim it as a "new low-cost objective measure for aphantasia", it should be remembered that this manuscript does not demonstrate the tool's efficacy in identifying individual subjects with aphantasia. The absence/presence of an imagery pupillary light response does not confirm/rule out aphantasia.

    Overall, the manuscript helps characterize an intriguing condition that until relatively recently received little empirical attention. These findings support the internal experiences described by aphantasic individuals, experiences that are often met with skepticism. Importantly, the authors have also offered the field a new objective physiological approximation of imagery vividness which can be incorporated into a number of study designs examining changes in imagery. The majority of previous measures relied on self-report alone and often suffered from the limitations of language (e.g., what it means for something to be "like vision" can be very different for different people). This manuscript also adds to the growing body of evidence of the power of internally generated signals, which can apparently reach all the way down the visual hierarchy to the eyes themselves.

  6. Version published to 10.1101/2021.09.02.457617v1 on bioRxiv