CE02 - Milieux et biodiversité : Terre vivante

COmparative MEntal Time Travel: insights from cephalopods – COMETT

Mental time travels in cephalopods

Mental time travel is considered as the ability to mentally travel backward or forward in time, re-experiencing past events, as well as imagining possible future ones. Evolutionary hypotheses have been stated by considering results of research in vertebrates, they are then difficult to test as their cognitive abilities may have evolved from common ancestors. Since the intelligence of modern cephalopod has arisen independently, they are highly promising species to study the evolution of MTT.

Aims of the projects

Aims of the project: <br /> <br />1) The first objective is to go further in the study of retrospective mental time travel in both cuttlefish and octopuses, by testing: 1) flexibility of episodic-like memory, a behavioural criterion which has not yet been tested; 2) source memory which has been suggested to allow vertebrates to differentiate one event from another. Answering this question will be helpful to better understand what aspects of mental time travel are similar or not in vertebrates and cephalopods. <br /> <br />2) The second major aim of our project is to test whether modern cephalopods possess future-planning abilities. This experiment will test the hypothesis that episodic memory has evolved to serve future planning. This will provide insights into understanding the link between retrospective and prospective mental time travel. <br /> <br />3) A mechanistic, bottom-up approach is needed, with a focus on exploring the neural underpinnings of an analogue of mental time travel in cephalopods, to pinpoint the neural machinery necessary for mental time travel.

The first two work packages of the project require the design of completely new behavioural procedures in both the common cuttlefish Sepia officinalis and the common octopus Octopus vulgaris. These cognitive tests will be useful to evaluate features of MTT abilities in cepahlopods:
- for episodic-like memory experiments: spatio-temporal context, flexibility, source of information
- for future planning: flexibility, independence of one's present motivational state

The third work package requires to design new methods (immunohistochemistry and in situ hybridization) to assess neuronal activation, via immediate early genes expression.

Results obtained between 01/2019 and 06/2020:

First experiments were realized in the common cuttlefish to better understand features of episodic-like memory in this species:

- Source memory: our results suggest that cuttlefish can retrieve perceptual features of a previous event, namely whether they had seen or smelled an item (Billard et al. 2020a)

- Flexibility: we showed that cuttlefish can adopt dynamic and flexible foraging behaviours including selective, opportunistic and future-dependent strategies, in response to changing foraging conditions. Cuttlefish restrain themselves from eating crabs (less preferred prey) for lunch when there will be shrimp (preferred prey) for dinner (Billard et al. 2020b)

Next experiments will focus on episodic-like memory in octopuses, and futur planning abilities in both cuttlefish and octopus. This will be useful to answer to the two following questions:
- is episodic-like memory a specific cognitive feature of cuttlefishes or is this cognitive ability shared among modern cephalopods?
- Possessing episodic-like memory abilities is or not indicative of futur planning abilities?

1. P. Billard, N.S. Clayton, C. Jozet-Alves (2020) Cuttlefish retrieve whether they smelt or saw a previously encountered item. Scientific reports 10:5413. DOI: 10.1038/s41598-020-62335-x

2. P. Billard, A.K. Schnell, N.S. Clayton, C. Jozet-Alves (2020) Cuttlefish show flexible and future-dependent foraging cognition. Biology Letters 16(2):20190743. DOI: 0.1098/rsbl.2019.0743

3. P. Billard, N.S. Clayton, C. Jozet-Alves (2019) Episodic memory. Encyclopedia of Animal Cognition and Behavior (J. Vonk & T. Shackelford eds.) Springer, Cham. DOI: 10.1007/978-3-319-47829-6_1770-1

Mental time travel (MTT) is considered as the human ability to mentally travel backward (i.e. episodic memory) or forward in time (i.e. foresight), re-experiencing past events, as well as imagining possible future ones. Episodic memory is defined as the recall of personally experienced events specifically referring to contextual information about what, where and when a particular event occurred. The non-human species in which episodic-like memory has been most thoroughly studied are California scrub-jays. Clayton and colleagues have indeed shown that they remember what, where, and when they have cached food and are able to flexibly use the memory of previously experienced cache events. As only behavioural criteria were used, this memory is referred as episodic-like memory. Source memory is another important aspect of episodic memory as it allows us to differentiate one episodic memory from another. It includes features (e.g. perceptual, contextual, temporal features) that were present when the episodic memory was formed. The prospective component of MTT, or foresight, is described as the ability of humans to flexibly anticipate their own mental states of need and act now to secure them. Some authors have stated that episodic memory has evolved to serve future planning. However, most hypotheses about the evolution of MTT have been stated by considering results of research in vertebrates. This makes evolutionary hypotheses difficult to test as their complex cognitive abilities may have evolved from common ancestors. It appears now necessary to use a more inclusive, comparative framework to better understand the Evolution of complex cognition. Since the intelligence of modern cephalopod molluscs (e.g. cuttlefish and octopuses) has arisen independently of the vertebrate lineage, they appear to be highly promising species to study MTT from evolutionary, mechanistic, functional and comparative perspectives. Recently, in collaboration with the Pr. Clayton, we have demonstrated that cuttlefish (cephalopod mollusc) keep track of what they have eaten, and where and how long ago they ate, in order to match their foraging behaviour with the time of replenishing of different foods. This cognitive ability fulfils the criteria of ‘what’, ‘where’ and ‘when’ of unique events and this study has provided the first behavioural evidence of episodic-like memory in an invertebrate. The COMETT project first aims to study episodic-like memory in another cephalopod species, the common octopus Octopus vulgaris, to determine whether this ability has specifically evolved in cuttlefish or whether it is more widely observed in modern cephalopods. This result will be helpful to determine the ecological pressures that have shaped this cognitive ability. In parallel, another feature of episodic-like memory will be tested in both cuttlefish and octopuses: source memory. Being in a comparative and evolutionary framework, showing both differences and similarities in the features of MTT between cephalopods and vertebrates is our prime concern. The second major aim of our project is to test whether modern cephalopods possess future-planning abilities. This experiment will test the hypothesis that episodic memory has evolved to serve future planning. Finally, a mechanistic, bottom-up approach will be realized, with a focus on exploring the neural underpinnings of episodic-like memory in cephalopods, to pinpoint the neural machinery necessary for MTT. Overall results of this project will facilitate the understanding of ecological pressures that may have led to the emergence of complex cognitive abilities in the animal kingdom.

Project coordinator

Madame Christelle Jozet-alves (Ethologie animale et humaine)

The author of this summary is the project coordinator, who is responsible for the content of this summary. The ANR declines any responsibility as for its contents.

Partner

Etho'S Ethologie animale et humaine

Help of the ANR 212,565 euros
Beginning and duration of the scientific project: December 2018 - 48 Months

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