Adaptive behavior and learning in slime moulds: the role of oscillations Aurèle Boussard, Adrian Fessel, Christina Oettmeier, Léa Briard, Hans-Gunther Dobereiner, Audrey Dussutour To cite this version: Aurèle Boussard, Adrian Fessel, Christina Oettmeier, Léa Briard, Hans-Gunther Dobereiner, et al.. Adaptive behavior and learning in slime moulds: the role of oscillations. Philosophical Transactions of the Royal Society of London. B (1887–1895), Royal Society, The, 2021. hal-02992905v1 HAL Id: hal-02992905 https://hal.archives-ouvertes.fr/hal-02992905v1 Submitted on 6 Nov 2020 (v1), last revised 25 Nov 2020 (v2) HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Submitted to Phil. Trans. R. Soc. B - Issue Adaptive behavior and learning in slime moulds: the role of oscillations Journal: Philosophical Transactions B Manuscript ID RSTB-2019-0757.R1 Article Type:ForReview Review Only Date Submitted by the n/a Author: Complete List of Authors: Boussard, Aurèle; CNRS, Research Center on Animal Cognition Fessel, Adrian; University of Bremen, Institut für Biophysik Oettmeier, Christina; University of Bremen, Institut für Biophysik Briard, Léa; CNRS, Research Center on Animal Cognition Döbereiner, Hans-Günther; University of Bremen, Institut für Biophysik Dussutour, Audrey; CNRS, Research Center on Animal Cognition Issue Code (this should have already been entered and appear below the blue box, BASAL but please contact the Editorial Office if it is not present): Subject: Behaviour < BIOLOGY, Biophysics < BIOLOGY, Cognition < BIOLOGY Physarum polycephalum, Slime mould, Learning, Cognition, Oscillations, Keywords: Synchronisation http://mc.manuscriptcentral.com/issue-ptrsb Page 1 of 27 Submitted to Phil. Trans. R. Soc. B - Issue 1 2 3 Author-supplied statements 4 5 6 Relevant information will appear here if provided. 7 8 Ethics 9 10 Does your article include research that required ethical approval or permits?: 11 This article does not present research with ethical considerations 12 13 Statement (if applicable): 14 CUST_IF_YES_ETHICS :No data available. 15 16 17 Data 18 19 It is a condition of publication that data, code and materials supporting your paper are made publicly 20 available. Does your paper present new data?: 21 My paper has no data For Review Only 22 23 Statement (if applicable): 24 25 CUST_IF_YES_DATA :No data available. 26 27 Conflict of interest 28 29 I/We declare we have no competing interests 30 31 Statement (if applicable): 32 CUST_STATE_CONFLICT :No data available. 33 34 35 Authors’ contributions 36 37 This paper has multiple authors and our individual contributions were as below 38 39 Statement (if applicable): 40 AB, AF and CO laid down the overall plan of the manuscript. AB, AF, CO, LB, HGD and AD contributed 41 to the first draft of the manuscript. AF, CO and AD produced the figures and the movies. AD 42 coordinated the writing of the article. AD and HGD secured funding. All authors gave final approval 43 44 for publication. 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 http://mc.manuscriptcentral.com/issue-ptrsb Submitted to Phil. Trans. R. Soc. B - Issue Page 2 of 27 1 Phil. Trans. R. Soc. B. article template 2 3 4 5 6 Phil. Trans. R. Soc. B. 7 8 doi:10.1098/not yet assigned 9 10 11 12 13 14 1 Adaptive behavior and learning in slime moulds: 15 16 17 18 2 the role of oscillations 19 20 1 2 2 1 21 3 Boussard Aurèle *, ForFessel AdrianReview*, Oettmeier Only Christina *, Briard Léa , 22 4 Döbereiner Hans-Günther2†, Dussutour Audrey1† 23 24 5 1Research Centre on Animal Cognition (CRCA), Centre for Integrative Biology (CBI), Toulouse University, 25 6 CNRS, UPS, Toulouse 31062, France. AD, 0000-0002-1377-3550 26 7 27 8 2Institut für Biophysik, Universität Bremen, Otto-Hahn-Allee 1, 28359 Bremen, Germany 28 9 29 10 * Co-first authors / Equal contribution / Names Listed in Alphabetical Order 30 11 31 12 †Authors for correspondence : [email protected] & [email protected] 32 13 33 34 14 Keywords: Physarum polycephalum, Slime mould, Learning, Cognition, Oscillations, Synchronisation 35 15 36 16 37 17 38 39 18 Summary 40 41 19 42 43 20 The slime mould Physarum polycephalum, an aneural organism, uses information from previous experiences to adjust 44 45 21 its behavior but the mechanisms by which this is accomplished remain unknown. This article examines the possible 46 22 role of oscillations in learning and memory in slime moulds. Slime moulds share surprising similarities with the 47 48 23 network of synaptic connections in animal brains. First, their topology derives from a network of interconnected, vein- 49 24 like tubes in which signalling molecules are transported. Second, network motility, which generates slime mould 50 51 25 behaviour, is driven by distinct oscillations that organize into spatiotemporal wave patterns. Likewise, neural activity 52 26 in the brain is organized in a variety of oscillations characterized by different frequencies. Interestingly, the oscillating 53 27 networks of slime moulds are not precursors of nervous systems but, rather, an alternative architecture. Here we argue 54 55 28 that comparable information processing operations can be realized on different architectures sharing similar oscillatory 56 29 properties. After describing learning abilities and oscillatory activities of P. polycephalum, we explore the relation 57 58 30 between network oscillations and learning, and evaluate the organisms global architecture with respect to information 59 60 1 http://mc.manuscriptcentral.com/issue-ptrsb Page 3 of 27 Submitted to Phil. Trans. R. Soc. B - Issue 1 2 3 4 31 processing potential. We hypothesize that, as in the brain, modulation of spontaneous oscillations may sustain learning 5 32 in slime mould. 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 For Review Only 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 http://mc.manuscriptcentral.com/issue-ptrsb Submitted to Phil. Trans. R. Soc. B - Issue Page 4 of 27 1 2 3 4 33 1. Introduction 5 6 7 34 Every living organism uses sensory and information-processing mechanisms to evaluate and interact with both 8 35 its internal milieu and its surroundings . Most processes underlying environmental monitoring, signal propagation or 9 36 integration of motor and sensory functions are evolutionary conserved between single-celled organisms and animals. 10 11 37 In this special issue, we emphasize that cognitive abilities such as perception, problem solving and learning are not 12 38 restricted to the animal kingdom, but have evolved in all organisms to satisfy the existential needs for survival [1–6]. 13 14 39 As Bourgine & Stewart [7] stated, “A system is cognitive if and only if sensory inputs serve to trigger actions in a 15 40 specific way, so as to satisfy a viability constraint”. Cognitive abilities rely on recursive chemical communication of 16 17 41 intracellular signalling networks which are highly organized in space and time and which depend on historical and 18 42 environmental context [8]. The functional link between dynamic processes in cells and their cognitive abilities 19 20 43 remains to be elucidated. One of the recurrent patterns observed in cells are self-sustained oscillations which can 21 44 encode various information [9–12].For The aim Review of this review is to discussOnly how learning in a unicellular organism might 22 45 rely on self-sustained oscillations. Our model system is the acellular slime mould Physarum polycephalum which 23 24 46 shows various oscillatory phenomena whose cognitive significance has yet to be demonstrated. 25 26 47 Learning, defined as the modification of behavior by experience, is one of the major innovations in the 27 48 evolution of life. Using past experiences is often critical for optimal decision-making in a fluctuating environment and 28 29 49 is involved in every aspect of an organism's life, including foraging and interacting with other individuals. We usually 30 50 think of learning as a trait that is limited to Neurozoans (i.e., organisms with a central nervous system). Indeed, learning 31 32 51 is often equated with neuronal changes like synaptic plasticity, implicitly precluding its existence in aneural organisms 33 52 such as plants and unicellulars [13]. While the evolutionary benefits of learning are clear, very little is known about 34 53 its origins. Even the simplest organisms must adapt to changing environments, raising the possibility that mechanisms 35 36 54 for learning might pre-date the evolution of nervous systems, possibly existing in a breadth of as-yet unstudied 37 55 organisms [3,5,6,14–19]. Evidence for learning in single-celled organisms remains scant and, to date, only few 38 39 56 unequivocal reports of such processes have been described. Learning in single-celled organisms has been investigated 40 57 mainly in ciliates and acellular slime moulds, and there are several reliable reports documenting learning in Stentor 41 42 58 sp. [20], Paramecium sp. [21], Tetrahymena sp. [22] and P. polycephalum [23]. 43 44 59 One of the most fundamental questions in cognitive science is: how can information inferred from interaction 45 60 with the physical world be encoded in physical/chemical changes in an organism, and how is it decoded as future 46 61 recall? Although many fundamental processes in the brain have been understood, the current state of the art in 47 48 62 neuroscience is still far from providing a complete picture.