Older adults detect happy facial expressions less rapidly

Previous experimental psychology studies based on visual search paradigms have reported that young adults detect emotional facial expressions more rapidly than emotionally neutral expressions. However, it remains unclear whether this holds in older adults. We investigated this by comparing the abilities of young and older adults to detect emotional and neutral facial expressions while controlling the visual properties of faces presented (termed anti-expressions) in a visual search task. Both age groups detected normal angry faces more rapidly than anti-angry faces. However, whereas young adults detected normal happy faces more rapidly than anti-happy faces, older adults did not. This suggests that older adults may not be easy to detect or focusing attention towards smiling faces appearing peripherally.

1. Authors have claimed that older adults have difficulty in detecting happy faces when it is not directly appearing in front of them. It implies that they do not have problems to detect a happy face when presented directly in front of them. Since they have not compared the detection of happy faces presented at the periphery compared to faces presented at the center of the screen, therefore, the authors need to be cautious in making such a conclusion. Alternatively, authors should find the previous literature where emotional faces were presented at the center of the screen, and they found the same results just like the current study. Authors can compare their results with previous studies to make such a claim.
2. The introduction is quite weak. For example, the authors were interested in comparing happy and angry emotions. However, in the introduction section, they have not mentioned the basic cognitive processing differences in the processing of happy and angry emotions (Gupta, 2019;Gupta et al., 2016). Also, a lot of literature is missing concerning emotion processing, specifically positive and negative emotion in general (Srinivasan & Gupta, 2010, 2011Gupta & Srinivasan, 2015, Gupta & Deak, 2015. Please add these studies and discuss them. Moreover, authors have not mentioned what could be the possible cognitive-affective mechanisms underlying the processing of happy and angry expressions that would have resulted in differences in young and old adults to process emotional stimuli. Many studies have shown that very little attention is required to process pleasant stimuli compared to unpleasant stimuli (see Gupta, 2019Gupta, , 2016Gupta et al., 2016;Srinivasan & Gupta, 2010, 2011Gupta & Srinivasan, 2015). 3. Authors have suggested that using anti-expression is more controlled stimuli compared to neutral stimuli. It is not very clear. 4. Please add some example of real faces (e.g., normal happy vs. anti happy face) used in the study. 5. It would be interesting to examine the detection RT/accuracy of emotional faces in the left vs. right visual field. It has been suggested that emotional face processing are right-hemisphere biased (see Gupta & Raymond, 2012;Gupta et al., 2018). This will give an insight into how emotions processing are represented in the old and young brain.

Review form: Reviewer 2
Is the manuscript scientifically sound in its present form? Yes

Recommendation?
Major revision is needed (please make suggestions in comments)

Comments to the Author(s)
In this behavioral study, Saito and colleagues compared the detection of angry and happy facial expressions (relative to neutral ones) between younger and older adults using a visual search task. The main finding is that older adults exhibited similar detection performance compared to younger ones in case of angry faces. However, the performance on happy faces differed between groups where older adults exhibited reduced detection performance. In general, the manuscript is well written, and the findings would be of interest to the affective neuroscience community. However, the authors should address the concerns noted below to clarify the design and interpretational issues further.
1. It is unclear why the authors had used only two facial stimuli though the Ekman face database contains stimuli from multiple actors? Because of this design choice, as the same target stimuli were repeated multiple (36) times across the experiment, could potential adaptation to happy faces in older adults explain the observed pattern of results?? 2. In the RT Results section, it was reported that the older adults exhibited better performance on anti-happy compared to anti-angry faces. Why should this be the case, especially when the authors stated earlier that the anti faces were typically perceived as neutral facial expressions?
3. In the Discussion section, the arguments of linking reduced social reward processing in older adults to the observed pattern of results are very speculative as no measures of social reward processing were collected and compared between the two groups. The authors should at least explicitly acknowledge that such a speculative hypothesis could be explicitly tested in future work.
4. In the Rating task, were the facial stimuli presented centrally or peripherally (as in the visual search task)? If presented centrally, how meaningful would be to relate them to the performance with peripherally presented faces in the visual search task (especially in the older adults)?? 5. It is a bit confusing to see the ANOVA findings based on the accuracy data under the Data Analyses section (page 15). It would be better if the authors could move them appropriately into the Results section.

12-Dec-2019
Dear Dr Saito, The editors assigned to your paper ("Older Adults Detect Happy Facial Expressions Less Rapidly") have now received comments from reviewers. We would like you to revise your paper in accordance with the referee and Associate Editor suggestions which can be found below (not including confidential reports to the Editor). Please note this decision does not guarantee eventual acceptance.
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• Funding statement Please list the source of funding for each author. Comments to the Author(s) The current paper aims to examine the detection of happy and angry emotions (controlling for visual properties) in young and old adults. Normal and anti-expression of angry and happy faces were presented as a target among neutral distractors in a visual search task. Both age groups were faster to detect faces with normal angry expression compared to faces with anti-angry expression. Young adults have also detected faces with a normal happy expression. However, older adults did not show the detection advantage for happy over anti-happy expression. This suggests that older adults may face difficulties in terms of quick detection and focusing attention toward smiling faces.
Overall, I liked the research question and methodology. However, I have a few concerns, which need to be resolved before publications.
1. Authors have claimed that older adults have difficulty in detecting happy faces when it is not directly appearing in front of them. It implies that they do not have problems to detect a happy face when presented directly in front of them. Since they have not compared the detection of happy faces presented at the periphery compared to faces presented at the center of the screen, therefore, the authors need to be cautious in making such a conclusion. Alternatively, authors should find the previous literature where emotional faces were presented at the center of the screen, and they found the same results just like the current study. Authors can compare their results with previous studies to make such a claim.
2. The introduction is quite weak. For example, the authors were interested in comparing happy and angry emotions. However, in the introduction section, they have not mentioned the basic cognitive processing differences in the processing of happy and angry emotions (Gupta, 2019;Gupta et al., 2016). Also, a lot of literature is missing concerning emotion processing, specifically positive and negative emotion in general (Srinivasan & Gupta, 2010, 2011Gupta & Srinivasan, 2015, Gupta & Deak, 2015. Please add these studies and discuss them. Moreover, authors have not mentioned what could be the possible cognitive-affective mechanisms underlying the processing of happy and angry expressions that would have resulted in differences in young and old adults to process emotional stimuli. Many studies have shown that very little attention is required to process pleasant stimuli compared to unpleasant stimuli (see Gupta

Reviewer: 2
Comments to the Author(s) In this behavioral study, Saito and colleagues compared the detection of angry and happy facial expressions (relative to neutral ones) between younger and older adults using a visual search task. The main finding is that older adults exhibited similar detection performance compared to younger ones in case of angry faces. However, the performance on happy faces differed between groups where older adults exhibited reduced detection performance. In general, the manuscript is well written, and the findings would be of interest to the affective neuroscience community. However, the authors should address the concerns noted below to clarify the design and interpretational issues further.

Comments to the Author(s)
Authors have incorporated all comments.

Review form: Reviewer 2
Is the manuscript scientifically sound in its present form? Yes

Comments to the Author(s)
The authors have done a great job in addressing my previous comments. I do not have any additional comments or concerns.

21-Feb-2020
Dear Dr Saito, It is a pleasure to accept your manuscript entitled "Older Adults Detect Happy Facial Expressions Less Rapidly" in its current form for publication in Royal Society Open Science. The comments of the reviewer(s) who reviewed your manuscript are included at the foot of this letter.
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Dear Dr. Narayanan Srinivasan and Essi Viding
We have uploaded the revised manuscript of "Older adults detect happy facial expressions less rapidly." We would like to thank the Associate Editor and the reviewers for reviewing our manuscript and giving us invaluable comments. We have revised the manuscript following your comments and major changes are highlighted. Additionally a professional Englishlanguage editing service made language-related changes, which are not highlighted unless the scientific content was altered.
We believe that the revised manuscript has improved thanks to your comments and suggestions. We would be grateful if you would consider this revised manuscript for publication in Royal Society Open Science.

Comment 1 Authors have claimed that older adults have difficulty in detecting happy faces when it is not
directly appearing in front of them. It implies that they do not have problems to detect a happy face when presented directly in front of them. Since they have not compared the detection of happy faces presented at the periphery compared to faces presented at the center of the screen, therefore, the authors need to be cautious in making such a conclusion. Alternatively, authors should find the previous literature where emotional faces were presented at the center of the screen, and they found the same results just like the current study. Authors can compare their results with previous studies to make such a claim.

Response
We agree with the reviewer on this point. Our results suggest that older adults may have difficulty detecting happy faces peripherally, therefore we have denoted this result and deleted the speculative expressions (in Abstract, Discussion, and Conclusion).

Comment 2
The introduction is quite weak. For example, the authors were interested in comparing happy and angry emotions. However, in the introduction section, they have not mentioned the basic cognitive processing differences in the processing of happy and angry emotions (Gupta, 2019;Gupta et al., 2016). Also, a lot of literature is missing concerning emotion processing, specifically positive and negative emotion in general (Srinivasan & Gupta, 2010, 2011Gupta & Srinivasan, 2015, Gupta & Deak, 2015. Please add these studies and discuss them.  Gupta, 2019Gupta, , 2016Gupta et al., 2016;Srinivasan & Gupta, 2010, 2011Gupta & Srinivasan, 2015).

Response
We have revised the Introduction section to cite studies that have examined the capturing power of positive (happy) stimuli (pages 5-6 in Introduction). Additionally, we have discussed the significance of positive stimuli on human beings and have interpreted our results as reflecting the decreased value of happy faces for older adults (page 18 in Discussion).

Comment 3
Authors have suggested that using anti-expression is more controlled stimuli compared to neutral stimuli. It is not very clear.

Response
Anti-expressions are not only generally rated as neutral expressions, but are also controlled stimuli for normal expressions in terms of visual (physical) characteristics of faces. In the previous version of the manuscript, we mentioned anti-expressions but failed to fully explain the term. In the revised manuscript, we have added the necessary explanation (page 3).

Comment 4
Please add some example of real faces (e.g., normal happy vs. anti happy face) used in the study.

Response
We cannot show real faces due to the lack of a license. Although all images published at Royal Society Open Science must be under the Creative Commons Attribution (CC BY) license (https://royalsociety.org/journals/authors/author-guidelines), the copyright for the images used in our study is held by The Paul Ekman Group, LLC and each reprint requires separate permission and payment. Therefore, we modified Figure 1 to show more realistic illustrations.

Comment 5
It would be interesting to examine the detection RT/accuracy of emotional faces in the left vs. right visual field. It has been suggested that emotional face processing are right-hemisphere biased (see Gupta & Raymond, 2012;Gupta et al., 2018). This will give an insight into how emotions processing are represented in the old and young brain.

Response
We conducted an ANOVA by adding the factor of visual field (right field versus left field).
Because the result did not show a significant four-way interaction (F(1,60) = 1.431, p >.10), we reported it as the result of preliminary analysis in the Materials and Methods section (page 13).

Comment 6
G-power analysis is required to determine the sample size.

Response
We have performed G-power analysis and described it in the Materials and Method section (pages 7-8).

Comment 7
Please address the theoretical and clinical implications of these results.

Response
We have discussed the implications of our results (pages 19-20 in Discussion).

Comment 1
It is unclear why the authors had used only two facial stimuli though the Ekman face database contains stimuli from multiple actors? Because of this design choice, as the same target stimuli were repeated multiple (36) times across the experiment, could potential adaptation to happy faces in older adults explain the observed pattern of results??

Response
The main reason that we did not use faces from other models is because it was not possible to create corresponding anti-expressions of anger and happiness from other models, particularly those with open mouths. We have made a reference to this limitation (pages 20-21 in Discussion).
Regarding the issue of the potential adaptation to happy faces, we examined whether adaptation effects would be observed. We conducted an ANOVA by adding the factor of presentation block. Because there was no significant four-way interaction (F(3,180) = 1.175, p >.10), we reported it as the result of preliminary analysis in the Materials and Methods section (page 13).

Comment 2
In the RT Results section, it was reported that the older adults exhibited better performance on anti-happy compared to anti-angry faces. Why should this be the case, especially when the authors stated earlier that the anti faces were typically perceived as neutral facial expressions?

Response
We have discussed this pattern of results by comparing them to the rating performance of these stimuli (pages 18-19 in Discussion).

Comment 3
In the Discussion section, the arguments of linking reduced social reward processing in older adults to the observed pattern of results are very speculative as no measures of social reward processing were collected and compared between the two groups. The authors should at least explicitly acknowledge that such a speculative hypothesis could be explicitly tested in future work.

Response
We did not conduct any tests related to social reward processing. Instead, we have attempted to explain our results using the hypotheses from studies that have examined the interaction between positive stimuli (including happy faces) and attention (page 18).

Comment 4
In the Rating task, were the facial stimuli presented centrally or peripherally (as in the visual search task)? If presented centrally, how meaningful would be to relate them to the performance with peripherally presented faces in the visual search task (especially in the older adults)??

Response
We have acknowledged that this is one of the limitations of our study and we have mentioned that presenting the faces in the same manner across the tasks would be necessary to examine the relationship between the performances of these tasks (page 20 in Discussion).

Comment 5
It is a bit confusing to see the ANOVA findings based on the accuracy data under the Data Analyses section (page 15). It would be better if the authors could move them appropriately into the Results section.

Response
We have updated the manuscript accordingly (page 15).