Interest in non-social novel stimuli as a function of age in rhesus monkeys

Human cognitive and affective life changes with healthy ageing; cognitive capacity declines while emotional life becomes more positive and social relationships are prioritized. This may reflect an awareness of limited lifetime unique to humans, leading to a greater interest in maintaining social relationships at the expense of the non-social world in the face of limited cognitive and physical resources. Alternately, fundamental biological processes common to other primate species may direct preferential interest in social stimuli with increasing age. Inspired by a recent study that described a sustained interest in social stimuli but diminished interest in non-social stimuli in aged Barbary macaques, we carried out a conceptual replication to test whether old rhesus monkeys lost interest in non-social stimuli. Male and female macaques (Macaca mulatta; N = 243) 4–30 years old were tested with a food puzzle outfitted with an activity monitor to evaluate their propensity to manipulate the puzzle in order to free a food reward. We found no indication that aged monkeys were less interested in the puzzle than young monkeys, nor were they less able to solve it.

2) Rearing conditions and species: The rhesus monkeys in the current study live in indoor cages either alone or in pairs, while in the original study Barbary macaque subjects lived in an outdoor enclosure in groups resembling rather natural conditions in terms of social life.
Given the absence of any assessments of social behavior and interest in social information the authors refer to a recent study of Rosati and colleagues and state that this one would "replicate" the effect of "sustained interest in social information by conspecifics (i.e., facial behaviors)" (Introduction page 3 l.43) -this not correct. Almeling et al did not find an effect of age on interest in playbacks of screams, photograph stimuli of neutral faces of conspecifics and frequency of "vocal commenting" on interactions of conspecifics. Rosati and colleagues addressed the question of whether Rhesus macaques have an increasing preferential interest with age for a) Positive over neutral and b) Neutral over negative facial expression and found evidence for a negativity bias with age (which is in contrast to previous observations in humans). In both of their experiments their analyses revealed that younger monkeys showed greater interest in the photographic stimuli than older monkeys.
As a whole, I appreciate the experimental design and study and would suggest the authors to submit in the "Article" section (focusing on cognitive aspects of aging rather than relating the study to social and socio-emotional aspects of aging).

06-Feb-2019
Dear Dr Bliss-Moreau, The Editors assigned to your Stage 1 Replication submission ("Interest in nonsocial novel stimuli as a function of age in rhesus monkeys") have now received comments from reviewers. We would like you to revise your paper in accordance with the referee and editors 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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Kind regards, Professor Chris Chambers Royal Society Open Science openscience@royalsociety.org on behalf of Chris Chambers (Registered Reports Editor, Royal Society Open Science) openscience@royalsociety.org Associate Editor Comments to Author (Professor Chris Chambers): Two expert reviewers have now appraised the manuscript. The reviewers differ markedly in their overall recommendations, with one recommending acceptance in principle (Reviewer 1) and the other recommending reject (Reviewer 2). The main objection of Reviewer 2 is that the study deviated substantially from the methodology of the original study and therefore fails to meet Stage 1 Criterion 2: "Whether the manuscript describes a sufficiently valid (i.e. close)...replication of the original study methods and rationale to provide an indication of replicability." I think there is merit in this criticism, and the authors may well agree given their labelling of the study as a conceptual replication. However, I would like to hear the authors' rebuttal on this point before making a final judgment.
Given the lack of other substantive criticisms, I will not reject the submission solely on the basis of the deviation from the original methodology. Instead, following the authors' response (and further editorial consideration), should the study be deemed to have fallen short of meeting Stage 1 Criterion 2, and should all other primary criteria be met, I will offer the authors the opportunity to publish the article as either a regular article or a Registered Report, where the condition of close replication does not apply. In this case the article would be offered in-principle acceptance via the Replications track, and would proceed as normal through the current workflow, but if/when accepted at Stage 2 would appear in either the Research Article or Registered Reports category.
Comments to Author: Reviewer: 1 Comments to the Author(s) I am very happy to see this conceptual replication of (parts of) our study, and I am eager to see the results. A minor issue: the hypotheses could be sharpened, and there is a typo on page 4, line 14 (double insertion of reference numbers). Regarding the discussion, I am sure that the authors will not only consider species differences but also substantial differences in housing conditions, with the Barbary macaques living in a large 20ha enclosure in near natural social groups while the rhesus monkeys in this study have little else to do. Yet, this does not constitute a criticism, just the encouragement to consider this in the discussion of variation in motivation in the two study populations. Best wishes, Julia Fischer Comments to the Author(s) This study by Bliss-Moreau and Baxter addresses the interest in manipulating a baited puzzle as well as the success rate in Rhesus macaques across adult ages. The sample size is substantial (N=243) and with the described statistical approach valid results were obtained. Accordingly, the study has the potential to contribute to our understanding of cognitive aging processes in NHPs regarding exploration, persistence and learning (speed).
For a number of reason I think this study is not suited to be published in the section "Replications". The authors state that they carried out a "conceptual replication" of a small part of a previous study from Almeling and colleagues -namely of whether old rhesus monkeys loose interest in nonsocial stimuli.
The journal, however, commits to publishing close replication attempts Among others, these are the main reason of why I think this study is not a close replication (of a part of the original study): 1) The task is highly different: In the current study the monkeys have to rotate the top over the bottom of the puzzle to be rewarded; several portions of rewards can be obtained within one trial. The monkeys were exposed to the task for 20 min and tested on two days. In the original study monkeys were tested only one time for approximately 2min in a problem-solving task involving food (plus two sorts of toys (not involving food)) and rewarded only one time in case they poked through paper tissue at the end of a tube and turned it so that the reward fell out. The reward obtained after one appropriate move by the monkey in the current study, may motivate subjects subsequent engagement with the puzzle, which I think is a crucial point in addition to the difference to the task as such.
The authors put some effort in making the analysis comparable to the one in the original study, e.g. they analyze monkeys exploratory tendency for the first two minutes (in addition to the analysis of the behavior in 20 min), and also they determine success on a yes/no basis (with more than 0 gram of reward obtained during 20 min trial counting as success) This is reasonable, taken that the authors aim to publish in the "Replication" section -but I do not feel it helps given the differences in the task. Further, I think this is unnecessary repeated testing of the same hypothesis.
2) Rearing conditions and species: The rhesus monkeys in the current study live in indoor cages either alone or in pairs, while in the original study Barbary macaque subjects lived in an outdoor enclosure in groups resembling rather natural conditions in terms of social life.
Given the absence of any assessments of social behavior and interest in social information the authors refer to a recent study of Rosati and colleagues and state that this one would "replicate" the effect of "sustained interest in social information by conspecifics (i.e., facial behaviors)" (Introduction page 3 l.43) -this not correct. Almeling et al did not find an effect of age on interest in playbacks of screams, photograph stimuli of neutral faces of conspecifics and frequency of "vocal commenting" on interactions of conspecifics. Rosati and colleagues addressed the question of whether Rhesus macaques have an increasing preferential interest with age for a) Positive over neutral and b) Neutral over negative facial expression and found evidence for a negativity bias with age (which is in contrast to previous observations in humans). In both of their experiments their analyses revealed that younger monkeys showed greater interest in the photographic stimuli than older monkeys.
As a whole, I appreciate the experimental design and study and would suggest the authors to submit in the "Article" section (focusing on cognitive aspects of aging rather than relating the study to social and socio-emotional aspects of aging).

20-Feb-2019
Dear Dr Bliss-Moreau On behalf of the Editor, I am pleased to inform you that your Manuscript RSOS-182237.R1 entitled "Interest in nonsocial novel stimuli as a function of age in rhesus monkeys" has been accepted in principle for publication in Royal Society Open Science.
As discussed, the central concern at Stage 1 was whether your replication protocol was sufficiently similar to the target study to meet Stage 1 Criterion 2: "Whether the manuscript describes a sufficiently valid (i.e. close) and robust (e.g. statistically powerful) replication of the original study methods and rationale to provide an indication of replicability". After reading (and in some cases re-reading) your paper, the target paper, the reviews received of your initial submission, and your response, I have decided that this criterion is sufficiently met for the article to continue as a Replication (and so without being transferred to a different article type). To explain further, Stage 1 Criterion 2 provides room for editorial discretion to permit deviations from the original methodology; in particular, what counts as "sufficiently close" to "provide an indication of replicability" is a subjective judgment. I was convinced that the similarity in methodology between your study and the target study is sufficiently high to "provide an indication of replicability", and I am persuaded that the rarity of replications (of any kind) in this field maximises both the value of the work and the editorial tolerance for deviations.
You may now progress to Stage 2 and complete the manuscript as approved.
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We encourage you to read the complete guidelines for authors concerning Stage 2 submissions at: http://rsos.royalsocietypublishing.org/page/replication-studies#AuthorsGuidance. Please especially note the requirements for data sharing and that withdrawing your manuscript will result in publication of a Withdrawn Registration.
Once again, thank you for submitting your manuscript to Royal Society Open Science and I look forward to receiving your Stage 2 submission. If you have any questions at all, please do not hesitate to get in touch. We look forward to hearing from you shortly with the anticipated submission date for your stage two manuscript.

Recommendation?
Accept with minor revision

Comments to the Author(s)
The results are pretty clear. I suggest however to rerun the analysis and include random slopes into the models. Not that this will greatly affect the results, but it is important to be correct. I was a bit puzzled why the results presented in Figure 3C did not reveal any significant age effect, given that the CI of the young and the old individuals did not overlap, but I trust the authors that this result is correct. Once the stats have been re-run, the paper can be accepted. The discussion is appropriately cautious. Overall, this is an important contribution to the literature.

23-Jul-2019
Dear Dr Bliss-Moreau On behalf of the Editor, I am pleased to inform you that your Stage 2 Replication submission RSOS-182237.R2 entitled "Interest in nonsocial novel stimuli as a function of age in rhesus monkeys" has been accepted for publication in Royal Society Open Science subject to minor revision in accordance with the referee suggestions. Please find the referees' comments at the end of this email.
The reviewers and Subject Editor have recommended publication, but also suggest some minor revisions to your manuscript. Therefore, I invite you to respond to the comments and revise your manuscript.
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When uploading your revised files please make sure that you have: 1) A text file of the manuscript (tex, txt, rtf, docx or doc), references, tables (including captions) and figure captions. Do not upload a PDF as your "Main Document". 2) A separate electronic file of each figure (EPS or print-quality PDF preferred (either format should be produced directly from original creation package), or original software format) 3) Included a 100 word media summary of your paper when requested at submission. Please ensure you have entered correct contact details (email, institution and telephone) in your user account 4) Included the raw data to support the claims made in your paper. You can either include your data as electronic supplementary material or upload to a repository and include the relevant DOI within your manuscript 5) Included your supplementary files in a format you are happy with (no line numbers, Vancouver referencing, track changes removed etc) as these files will NOT be edited in production The Stage 2 manuscript was returned to both reviewers who assessed the manuscript at Stage 1. One reviewer was not available. Based on the available reviewer's assessment, and my own reading of the manuscript, I have decided to proceed without further in-depth review. As you will see, the reviewer is satisfied with the Stage 2 submission but recommends an additional analysis in the interests of robustness. Since this deviates from the approved methodology at Stage 1 (and deviations from analysis plans, especially, are unusual in Stage 2 Replications), I am not going to require it --however I would encourage the authors to consider the suggestion carefully. The analysis could be reported briefly as an additional unregistered analysis or unregistered robustness check.
Reviewers' comments to Author: Reviewer: 1 Comments to the Author(s) The results are pretty clear. I suggest however to rerun the analysis and include random slopes into the models. Not that this will greatly affect the results, but it is important to be correct. I was a bit puzzled why the results presented in Figure 3C did not reveal any significant age effect, given that the CI of the young and the old individuals did not overlap, but I trust the authors that this result is correct. Once the stats have been re-run, the paper can be accepted. The discussion is appropriately cautious. Overall, this is an important contribution to the literature.

Julia Fischer
Author's Response to Decision Letter for (RSOS-182237.R2) See Appendix C.

12-Aug-2019
Dear Dr Bliss-Moreau: It is a pleasure to accept your Stage 2 Replication entitled, "Interest in nonsocial novel stimuli as a function of age in rhesus monkeys" in its current form for publication in Royal Society Open Science.
Thank you for your fine contribution. On behalf of the Editors of Royal Society Open Science, we look forward to your continued contributions to the Journal.