Episodic-like memory is preserved with age in cuttlefish

Episodic memory, remembering past experiences based on unique what–where–when components, declines during ageing in humans, as does episodic-like memory in non-human mammals. By contrast, semantic memory, remembering learnt knowledge without recalling unique what–where–when features, remains relatively intact with advancing age. The age-related decline in episodic memory likely stems from the deteriorating function of the hippocampus in the brain. Whether episodic memory can deteriorate with age in species that lack a hippocampus is unknown. Cuttlefish are molluscs that lack a hippocampus. We test both semantic-like and episodic-like memory in sub-adults and aged-adults nearing senescence (n = 6 per cohort). In the semantic-like memory task, cuttlefish had to learn that the location of a food resource was dependent on the time of day. Performance, measured as proportion of correct trials, was comparable across age groups. In the episodic-like memory task, cuttlefish had to solve a foraging task by retrieving what–where–when information about a past event with unique spatio-temporal features. In this task, performance was comparable across age groups; however, aged-adults reached the success criterion (8/10 correct choices in consecutive trials) significantly faster than sub-adults. Contrary to other animals, episodic-like memory is preserved in aged cuttlefish, suggesting that memory deterioration is delayed in this species.

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Do you have any ethical concerns with this paper? Yes
Comments to the Author I read the manuscript "Episodic-like memory is preserved with age in cuttlefish" and found it an interesting study exploring episodic memory in the cephalopod mollusc Sepia officinalis.
First of all, I have to say that despite the study does not require ethical approval because experiments on live animals have been carried out in the USA, there are important details about care, maintenance and use of live animals for research purposes that should be reported. This is mandatory according to ARRIVE Guidelines -that this Journal and the Royal Society that states "Authors are expected to comply with the 'Animal Research: Reporting In Vivo Experiments' (ARRIVE) guidelines. These have been developed by NC3Rs to improve standards of reporting to ensure that the data from animal experiments can be fully scrutinised and utilised. Relevant information should be included in the appropriate section of the article, as outlined in the ARRIVE guidelines" (see https://royalsociety.org/journals/ethics-policies/research-ethics/). I strongly recommend the Authors to revise their manuscript attentively, in order to report all the necessary details about this study as required by ARRIVE Checklist and the best practice of in vivo studies reporting (see also PREPARE: Smith, A.J., Clutton, R.E., Lilley, E., Hansen, K.E. A., and Brattelid, T. (2018). PREPARE: guidelines for planning animal research and testing. Laboratory Animals 52(2), 135-141. doi: 10.1177/0023677217724823.). I recommend to provide details (to mention some) about: i. the individual/group housing of the animals between experimental trials; ii. body size of the animals (in addition to age group); iii. size and shape and all required details about the holding and experimental tanks; iv. monitoring of seawater quality, v. number of subjects excluded (if any).
I would like also to remind that following the "Guidelines for the treatment of animals in behavioural research and teaching" studies carried out using captive animals "may mean obtaining them from the wild and necessarily involve confinement" require attention in assuring best practice and compliance with the principles of keeping animals in an optimal welfare status, including manipulation/handling. This reviewer is fully aware of the long, well established, consolidated practice in housing live cephalopods at the MBL, but I reiterate that the overall quality of the scientific work using these species will enormous improve if transparency about animal care and maintenance and details about experimental settings will be provided, despite not required by legislation in non-EU countries.
The study is an interesting one exploring time-age capacity for episodic and semantic memories in the cuttlefish. As reported by Authors, known age-related decline in episodic memory "is thought to stem from deteriorating function of the hippocampus in the brain. Whether episodic memory can deteriorate with age in species that lack a hippocampus". Testing this research question in cuttlefish offers interesting advantages. Authors tested semantic-and episodic-like memories in sub-adults and aged cuttlefish. The semantic-like memory task was designed to let the animal to learn that the location of a food resource in relation with the time of the day. In the episodic-like memory task, the paradigm designed required the solution of a foraging task (what-where-when information about a past event with unique spatiotemporal features). Performance of the semantic-like memory task resulted comparable across age groups. However, with the episodic memory Authors found that aged-adults reached the success criterion faster than sub-adults. Authors conclude that contrary to what known in other species, episodic-like memory is preserved in aged cuttlefish, "suggesting that memory deterioration is delayed in this species".
Independently from what anticipated in the previous paragraphs, I am in the unfortunate situation of not being able to recommend the acceptance of the manuscript in its current form. I am going to provide the following comments for Authors to consider in their substantial revision.
2. Selection criteria of aged individuals. Authors report (lines 148-150) that "Aged cuttlefish that showed obvious signs of senescence were chosen for both memory experiments. These signs included a decrease in appetite, irregular flickering of chromatophore skin cells, and a decrease in reaction rate to visual stimuli." The Reader asks 2.1 the paradigms utilized require that the animal will make association between a visual stimulus and an 'edible' reward. Thus, how the choice of the test is compatible with the animal "status" and effective capability? 2.2 Authors report that animal are fed ad libitum. Authors should specify better how this is done; ad libitum means that food items are always available to the animals and this does not allow control of the amount of food taken by single individual (for example). There is no information whether before pre-training and testing phases cuttlefish have been food-deprived.
3. "we trained cuttlefish to approach a specific location in their tank" (line 152). Size of the tank is missing, relative size when referred to number/body size of animals, home position of the animals during the test in relationship with the location of the "places" 4. It is not clear enough whether the paradigm described at (c) semantic-like memory is also referring to episodic memory. Authors should provide clear distinction in the way the tests have been designed. The confusion also emerges when reading the Discussion (lines 304-305) "…Specifically, they were able to remember what they had eaten for breakfast, where they had eaten it, and how long ago" where the authors refer to the other one. 5. Authors do not have any indication of the status of neural circuit in the animals utilized (see also above) and in absence of details about individual performances and behavioral locomotory and other responses it is difficult to generalize the conclusions. I suggest in any case to revise the Discussion in order to take into account the above comments.

Review form: Reviewer 2
Recommendation Accept with minor revision (please list in comments)

Scientific importance: Is the manuscript an original and important contribution to its field? Excellent
General interest: Is the paper of sufficient general interest? Excellent Quality of the paper: Is the overall quality of the paper suitable? Excellent

Is the length of the paper justified? Yes
Should the paper be seen by a specialist statistical reviewer? No Do you have any concerns about statistical analyses in this paper? If so, please specify them explicitly in your report.

No
It is a condition of publication that authors make their supporting data, code and materials available -either as supplementary material or hosted in an external repository. Please rate, if applicable, the supporting data on the following criteria.

Comments to the Author
The manuscript reports an interesting study focused on the potential age-related decline in measures of episodic and sematic memory in cuttlefish. The main finding is that measures of episodic and semantic memory do not decline with age in cuttlefish. The observation that episodic memory is intact at an advanced age is important for understanding the evolution of cognition and potentially opening a new model system for understanding the mechanisms that preserve this otherwise fragile memory system. I recommend that the manuscript be published after the authors address some minor issues described below.
The authors should comment on the comparability of the semantic and episodic tasks. In some respects, the what-where-when task is more complicated as it depends on item-specific information. Yet, the semantic task used 3 times of day whereas the episodic task used 2 delay conditions. It may not be possible to fully equate the tasks, but the authors should at least comment on the issue. Your manuscript has now been peer reviewed and the reviews have been assessed by an Associate Editor. The reviewers' comments (not including confidential comments to the Editor) and the comments from the Associate Editor are included at the end of this email for your reference. The reviewers and the Associate Editor and I all find quite a lot to like about your manuscript, however there were several critical issues raised that must be addressed before your manuscript can be considered further. All of these are well explained by the reviewers and nicely summarized by the AE, but to reiterate the key issues, it is necessary to include the details of the animals' husbandry and the experimental procedure, the former because we require compliance with the ARRIVE guidelines (independent of the scientists' home country guidelines) and second because right now there are not sufficient details to fully determine how the study was run. In addition, I agree with the AE that the paper will be greatly strengthened by a consideration of the cuttlefishes' natural history and some consideration of why this ability may have evolved.
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Thank you for submitting your manuscript to Proceedings B; we look forward to receiving your revision. If you have any questions at all, please do not hesitate to get in touch.
Best wishes, Dr Sarah Brosnan Editor, Proceedings B mailto: proceedingsb@royalsociety.org Associate Editor Comments to Author: Two reviewers have provided feedback on your submission and while both were in agreement that your study offers novel and interesting findings, both also ask for some revisions and clarifications.
In particular I wish to highlight the comments from Reviewer 1 who calls for greater detail in terms of your methodology and who proposes that the ARRIVE guidelines should be used as a template here (this journal promotes the use of the ARRIVE guidelines for reporting animal subjects research). I am in complete agreement with this that additional detail is required not only to understand the welfare and husbandry of the study subjects but also to facilitate reproducibility of your study protocols. For example, please describe how you trained the subjects (2b) -what training methods did you use? how long were training sessions? How many training sessions did subjects require on average and what was the variation across subjects? did you train subjects singly? Similarly, for the testing protocol, while you provide some aspects of the methods (e.g., how far apart the feeding stations were) other elements (such as tank size, stimuli size etc.) were lacking. I think some more detailed schematics in addition to the current Fig 1 might help. Finally, and while you touch on this in your introduction, I think your Discussion would benefit from a more detailed consideration of the evolutionary processes that might have shaped the results you find i.e. what is it about the cuttlefishes natural history and native ecology or sociality that might help interpret these results. This broader perspective -beyond narrowly focussing on the cognitive underpinnings -would be welcome given the broad scope of this journal.
Reviewer(s)' Comments to Author: Referee: 1 Comments to the Author(s) I read the manuscript "Episodic-like memory is preserved with age in cuttlefish" and found it an interesting study exploring episodic memory in the cephalopod mollusc Sepia officinalis.
First of all, I have to say that despite the study does not require ethical approval because experiments on live animals have been carried out in the USA, there are important details about care, maintenance and use of live animals for research purposes that should be reported. This is mandatory according to ARRIVE Guidelines -that this Journal and the Royal Society that states "Authors are expected to comply with the 'Animal Research: Reporting In Vivo Experiments' (ARRIVE) guidelines. These have been developed by NC3Rs to improve standards of reporting to ensure that the data from animal experiments can be fully scrutinised and utilised. Relevant information should be included in the appropriate section of the article, as outlined in the ARRIVE guidelines" (see https://royalsociety.org/journals/ethics-policies/research-ethics/). I strongly recommend the Authors to revise their manuscript attentively, in order to report all the necessary details about this study as required by ARRIVE Checklist and the best practice of in vivo studies reporting (see also PREPARE: Smith, A.J., Clutton, R.E., Lilley, E., Hansen, K.E.A., and Brattelid, T. (2018). PREPARE: guidelines for planning animal research and testing. Laboratory Animals 52(2), 135-141. doi: 10.1177/0023677217724823.). I recommend to provide details (to mention some) about: i. the individual/group housing of the animals between experimental trials; ii. body size of the animals (in addition to age group); iii. size and shape and all required details about the holding and experimental tanks; iv. monitoring of seawater quality, v. number of subjects excluded (if any).
I would like also to remind that following the "Guidelines for the treatment of animals in behavioural research and teaching" studies carried out using captive animals "may mean obtaining them from the wild and necessarily involve confinement" require attention in assuring best practice and compliance with the principles of keeping animals in an optimal welfare status, including manipulation/handling. This reviewer is fully aware of the long, well established, consolidated practice in housing live cephalopods at the MBL, but I reiterate that the overall quality of the scientific work using these species will enormous improve if transparency about animal care and maintenance and details about experimental settings will be provided, despite not required by legislation in non-EU countries.
The study is an interesting one exploring time-age capacity for episodic and semantic memories in the cuttlefish. As reported by Authors, known age-related decline in episodic memory "is thought to stem from deteriorating function of the hippocampus in the brain. Whether episodic memory can deteriorate with age in species that lack a hippocampus". Testing this research question in cuttlefish offers interesting advantages. Authors tested semantic-and episodic-like memories in sub-adults and aged cuttlefish. The semantic-like memory task was designed to let the animal to learn that the location of a food resource in relation with the time of the day. In the episodic-like memory task, the paradigm designed required the solution of a foraging task (what-where-when information about a past event with unique spatiotemporal features). Performance of the semantic-like memory task resulted comparable across age groups. However, with the episodic memory Authors found that aged-adults reached the success criterion faster than sub-adults. Authors conclude that contrary to what known in other species, episodic-like memory is preserved in aged cuttlefish, "suggesting that memory deterioration is delayed in this species".
Independently from what anticipated in the previous paragraphs, I am in the unfortunate situation of not being able to recommend the acceptance of the manuscript in its current form. I am going to provide the following comments for Authors to consider in their substantial revision.
2. Selection criteria of aged individuals. Authors report (lines 148-150) that "Aged cuttlefish that showed obvious signs of senescence were chosen for both memory experiments. These signs included a decrease in appetite, irregular flickering of chromatophore skin cells, and a decrease in reaction rate to visual stimuli." The Reader asks 2.1 the paradigms utilized require that the animal will make association between a visual stimulus and an 'edible' reward. Thus, how the choice of the test is compatible with the animal "status" and effective capability? 2.2 Authors report that animal are fed ad libitum. Authors should specify better how this is done; ad libitum means that food items are always available to the animals and this does not allow control of the amount of food taken by single individual (for example). There is no information whether before pre-training and testing phases cuttlefish have been food-deprived.
3. "we trained cuttlefish to approach a specific location in their tank" (line 152). Size of the tank is missing, relative size when referred to number/body size of animals, home position of the animals during the test in relationship with the location of the "places" 4. It is not clear enough whether the paradigm described at (c) semantic-like memory is also referring to episodic memory. Authors should provide clear distinction in the way the tests have been designed. The confusion also emerges when reading the Discussion (lines 304-305) "…Specifically, they were able to remember what they had eaten for breakfast, where they had eaten it, and how long ago" where the authors refer to the other one. 5. Authors do not have any indication of the status of neural circuit in the animals utilized (see also above) and in absence of details about individual performances and behavioral locomotory and other responses it is difficult to generalize the conclusions. I suggest in any case to revise the Discussion in order to take into account the above comments.
Referee: 2 Comments to the Author(s) The manuscript reports an interesting study focused on the potential age-related decline in measures of episodic and sematic memory in cuttlefish. The main finding is that measures of episodic and semantic memory do not decline with age in cuttlefish. The observation that episodic memory is intact at an advanced age is important for understanding the evolution of cognition and potentially opening a new model system for understanding the mechanisms that preserve this otherwise fragile memory system. I recommend that the manuscript be published after the authors address some minor issues described below.
The authors should comment on the comparability of the semantic and episodic tasks. In some respects, the what-where-when task is more complicated as it depends on item-specific information. Yet, the semantic task used 3 times of day whereas the episodic task used 2 delay conditions. It may not be possible to fully equate the tasks, but the authors should at least comment on the issue. Decision letter (RSPB-2021-1052.R1)

12-Jul-2021
Dear Dr Schnell I am pleased to inform you that your manuscript RSPB-2021-1052.R1 entitled "Episodic-like memory is preserved with age in cuttlefish" has been accepted for publication in Proceedings B pending some minor revisions, listed below. I invite you to respond to the referee(s)' comments and revise your manuscript. Because the schedule for publication is very tight, it is a condition of publication that you submit the revised version of your manuscript within 7 days. If you do not think you will be able to meet this date please let us know.
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Sincerely, Proceedings B mailto: proceedingsb@royalsociety.org Associate Editor: Comments to Author: Thank you very much for making all of the suggested edits and clarifications that I proposed.

Manuscript ID RSPB-2021-1052
Episodic-like memory is preserved with age in cuttlefish Thank you for inviting us to revise this manuscript. We have conducted revisions and believe that our manuscript has improved thanks to the constructive feedback provided by the editor and the reviewersfor this we are grateful and thank them for their time and effort. For your reference, we have provided a response below each of the reviewers' comments.
Associate Editor Comments to Author: Two reviewers have provided feedback on your submission and while both were in agreement that your study offers novel and interesting findings, both also ask for some revisions and clarifications.
In particular I wish to highlight the comments from Reviewer 1 who calls for greater detail in terms of your methodology and who proposes that the ARRIVE guidelines should be used as a template here (this journal promotes the use of the ARRIVE guidelines for reporting animal subjects research). I am in complete agreement with this that additional detail is required not only to understand the welfare and husbandry of the study subjects but also to facilitate reproducibility of your study protocols. For example, please describe how you trained the subjects (2b) -what training methods did you use? how long were training sessions? How many training sessions did subjects require on average and what was the variation across subjects? did you train subjects singly? Similarly, for the testing protocol, while you provide some aspects of the methods (e.g., how far apart the feeding stations were) other elements (such as tank size, stimuli size etc.) were lacking. I think some more detailed schematics in addition to the current Fig 1 might help. Authors' response: Thanks for these insightful comments. To show that our practices coincide with ARRIVE guidelines we have added extra details in our methods section as electronic supplementary material. We have also added more details about our training processes to facilitate reproducibility of our study protocols, these can be found in the electronic supplementary materials. Finally, we have added an extra schematic figure to help readers visualise our methods in the semantic-like memory task (see Figure 1).

Finally, and while you touch on this in your introduction, I think your
Discussion would benefit from a more detailed consideration of the evolutionary processes that might have shaped the results you find i.e., what is it about the cuttlefishes natural history and native ecology or sociality that might help interpret these results. This broader perspective -beyond narrowly focussing on the cognitive underpinnings -would be welcome given the broad scope of this journal. Authors' response: We have devoted a paragraph on this subject previously in the discussion section (see lines: 373-394) and we believe it is sufficient coverage for this issue lest it become too speculative. Specifically, we argue that resistance to age-related decline to preserve complex learning and memory might have been positively selected for because it enables individuals to recall specific spatiotemporal