Performance of goats in a detour and a problem-solving test following long-term cognitive test exposure

Cognitive research in long-lived species commonly involves using the same animals in different experiments. It is unclear whether the participation in cognitive tests can notably alter the performance of individuals in subsequent conceptually different tests. We therefore investigated whether exposure to cognitive tests affects future test performance of goats. We used three treatment groups: goats with long-term exposure to human-presented object-choice tests (for visual discrimination and reversal learning tests + cognitive test battery), goats that were isolated as for the test exposure but received a reward from the experimenter without being administered the object-choice tests, and goats that were isolated but neither received a reward nor were administered the tests. All treatment groups were subsequently tested in two conceptually different cognitive tests, namely a spatial A-not-B detour test and an instrumental problem-solving test. We tested dairy goats, selected for high productivity, and dwarf goats, not selected for production traits, each at the same two research sites. We did not find notable differences between treatments with respect to the goats' detour or problem-solving performance. However, high variation was observed between the research sites, the selection lines, and among individuals, highlighting potential pitfalls of making accurate comparisons of cognitive test performances.


Decision letter (RSOS-210656.R0)
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Both Reviewers concur with us that this is a good piece of work which we would like to accept.
Both reviewers make some useful suggestions to strengthen the ms. We would like those to be taken into account in your revision. Most of these comments are both substantive yet easily addressed. For example see Rev 1 L359 comment. The care you have taken in your work is noted by the Reviewers who have done a great job of reading and responding to the ms in detail.
Reviewer comments to Author: Reviewer: 1 Comments to the Author(s) This manuscript aims at investigating the effect of previous exposure to training, including isolation from other individual, food rewards provided by humans and cognitive tests, on performance of 2 goat lines (dwarf and dairy) during 2 standard cognitive tasks (detour and instrumental problem-solving test). The results do not show any clear treatment effects, but point towards selection line differences for instance. These results provide valuable knowledge on the impact (or absence of impact) of former training in farm animals used in cognitive research. I have a suggestion for further tests and comments on the design and statistics.
As a general comment, if the authors are interested in differences between selection lines, which have been bred based on various characteristics for several generations, they should maybe consider adding the selection line as an addition fixed effect in their models. This would allow a more direct comparison of performances between lines, which would be very interesting.
L210-214. Were ISO goats exposed to humans during the isolation (was an experimenter present)?
L326-338. The number of animals excluded is unusually high. Aren't the results of some of these excluded animals relevant (e.g. number of goats that didn't perform the task within 60s, or that didn't perform correctly in A3 and A4)?
L359. If I understand correctly, your model doesn't include the main effects alone (Type and Treatment) and instead only includes their interaction? Normally, interactions should not be included in a model without the corresponding main effects.
Reviewer: 2 Comments to the Author(s) Please see the attached file "RSOS-210656 review.pdf".

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Author's Response to Decision Letter for (RSOS-210656.R0) Decision letter (RSOS-210656.R1) We hope you are keeping well at this difficult and unusual time. We continue to value your support of the journal in these challenging circumstances. If Royal Society Open Science can assist you at all, please don't hesitate to let us know at the email address below.
Dear Mrs Rosenberger, I am pleased to inform you that your manuscript entitled "Performance of goats in a detour and a problem-solving test following long-term cognitive test exposure." is now accepted for publication in Royal Society Open Science.
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On behalf of the Editors of Royal Society Open Science, thank you for your support of the journal and we look forward to your continued contributions to Royal Society Open Science. This is a valuable manuscript. It reports a well-designed and well-conducted experiment, with a substantial sample size, to investigate a question that is important but might be thought a little dull -does exposing the same individuals to repeated cognitive testing affect their performance on those tests, even if the tests concerned are apparently unrelated? As the authors document, it is common practice in animal cognition to test the same individuals repeatedly, and the longer-lived and more exotic and expensive the species concerned, the more likely this is to happen. Given that longerlived, exotic and expensive species are often those of most scientific and public interest, the question is an acute one.
The strengths of the paper lie in the facts that (a) the authors carefully considered what factors might contribute to an apparent improvement in performance with repeated testing, so they included control groups that experienced some of the manipulations involved in testing but not the tests themselves; and (b) they included some ecologically valid variations between groups -two different cognitive tests, different strains, and different testing sites -of the sort that inevitably arise when we compare experiments by different research groups.
As it turned out, the authors found that previous testing experience did not have any effect on performance in their final tests, whereas both strain and test site did, at least on one of their tests (PST, a problem-solving test involving removing a lid from a familiar food container); there was also great individual variation. Again, that might be thought a dull result. On the contrary, it's very important -and a huge relief to those of us who have spent much time testing the same few animals in different experiments.
In addition to the merits of the experiments and the results, the Introduction provides a valuable review of the existing literature on the impacts on animals of cognitive testing, and the procedures associated with it.
The paper is clearly and professionally written. I only have two concerns about the information provided, and one is trivial. 1. In the PST, I could not find it stated whether the food container was fixed, to the ground or the wall of the enclosure. This makes quite a difference to the possible manipulations the goats could have used to dislodge the lid. 2. The only suggestion of an effect of previous cognitive training was in the A-not-B detour test (ABT), where goats with prior cognitive experience (COG group) showed a significant improvement in performance across the four trials in the B condition, whereas other goats did not (although the trend was in the same direction), and this is discussed as indicated that perhaps the COG groups learned faster (lines 398-400, 487-489). Comparing statistical significance levels in this way is an error: difference of significance does not indicate significance of difference. The appropriate procedure is to carry out a test of the interaction between trial number and experience group. From the formula in lines 359-360, I don't think such an interaction was included in the model (though I

Appendix A
am not an expert in R model formulae). If the authors want to examine learning rates, they need to include interactions in their model. They also need to show us the trends in proportions of trials correct as a function of trial number -it would be possible for the trend to be identical in the three experience groups, and yet for there to be a difference in significance, because of differences in individual variation.
As an aside, the need for goats to manipulate specific plants (lines 562-563) is interesting, and put me in mind of Byrne's studies of gorilla food technology (e.g. Byrne & Byrne 1993, Amer J Primatology). It's probably too remote a connection to bring into the paper, however.
As regards presentation, I only have one substantive suggestion. At line 135, the authors don't quite bring out that using two different research sites is a strength of their design (though they recognize this at lines 146-148). I suggest changing "the same two" in line 135 to "two different" to make the point.
The English of the paper is excellent, clear, unfussy and almost entirely correct. In just a few places it isn't quite idiomatic. I noticed the following places where the authors could make the text sound more natural. I am sure there are other similar instances, but these points are so minor that further copy-editing is quite unnecessary.

Line 29
"conditioned" is odd. More natural would be "used" 53 "the participation" -drop "the" 61 "The frequent" -drop "The" 71 "hardly" isn't quite right. You could say "hardly at all" but that would be fussy. The best word in context is probably "barely". 77 change "have not been" to "was" 150 insert "a" before "pet" 153 change "does likely not exceed" to "probably does not exceed" 197 delete "à" 204 Are you American or European? In this sort of context, Americans use singular verbs after "group" (because there's just one group); European English speakers use plural verbs (because there are multiple individuals in the group). Take your choice! 332 Change "per definition" to "by definition" 545 Change "chicken" to "chickens" 549 Change "As it is common" to "As is common"

Response to reviewer
Dear Editor, Thank you for the thoughtful and constructive comments from you and the two reviewers on our manuscript 'Performance of goats in a detour and a problem-solving test following longterm cognitive test exposure.' As requested, we have revised the manuscript, taking careful account of all comments made by yourself and the two reviewers. Together with this revision note, we have resubmitted a revised version of the manuscript with all changes highlighted.
We hope that the present version of the manuscript has improved significantly and that you might consider this manuscript now for publication in Royal Society Open Science.
The material in this manuscript has not been published elsewhere and is not submitted for publication elsewhere. All authors have seen the final manuscript and we all take responsibility for its contents.
Sincerely, Katrina Rosenberger, Michael Simmler, Jan Langbein, Nina Keil and Christian Nawroth, Performance of goats in a detour and a problem-solving test following long-term cognitive test exposure Response to reviewers Reviewer Comments:

Reviewer 1
This manuscript aims at investigating the effect of previous exposure to training, including isolation from other individual, food rewards provided by humans and cognitive tests, on performance of 2 goat lines (dwarf and dairy) during 2 standard cognitive tasks (detour and instrumental problem-solving test). The results do not show any clear treatment effects, but point towards selection line differences for instance. These results provide valuable knowledge on the impact (or absence of impact) of former training in farm animals used in cognitive research. I have a suggestion for further tests and comments on the design and statistics.
Authors' response: Thank you for the positive feedback!
As a general comment, if the authors are interested in differences between selection lines, which have been bred based on various characteristics for several generations, they should maybe consider adding the selection line as an addition fixed effect in their models. This would allow a more direct comparison of performances between lines, which would be very interesting.
Authors' response: More than one selection line were included in our study to increase heterogeneity among goats in order to get a more robust inference towards our effects of interest, which are the treatment effects (see description of goals in introduction).
During the design of the study, we did not anticipate to compare the performance of both selection lines and think that adding this term ad hoc as additional fixed effect would be a deviation from the initial study rational. We think our models best reflect our initial intention.
L210-214. Were ISO goats exposed to humans during the isolation (was an experimenter present)?
Authors' response: We rephrased the text accordingly.
Line 210-215: "Individuals allocated to the ISO treatment neither participated in cognitive tests nor did they receive rewards by the experimenter. However, they were isolated over a similar period as the COG and the POS group in the same arena (= median time taken by COG group to finish all trials in the previous test session) and with the experimenter present behind the crate, as was the case for the COG and POS treatments." L326-338. The number of animals excluded is unusually high. Aren't the results of some of these excluded animals relevant (e.g. number of goats that didn't perform the task within 60s, or that didn't perform correctly in A3 and A4)?