Steps towards a computational ethology: an automatized, interactive setup to investigate filial imprinting and biological predispositions.
Automated setup
Chicks
Imprinting
Innate behaviour
Matlab
Predispositions
Journal
Biological cybernetics
ISSN: 1432-0770
Titre abrégé: Biol Cybern
Pays: Germany
ID NLM: 7502533
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
received:
05
05
2021
accepted:
06
07
2021
pubmed:
18
7
2021
medline:
6
5
2022
entrez:
17
7
2021
Statut:
ppublish
Résumé
Soon after hatching, the young of precocial species, such as domestic chicks or ducklings, learn to recognize their social partner by simply being exposed to it (imprinting process). Even artificial objects or stimuli displayed on monitor screens can effectively trigger filial imprinting, though learning is canalized by spontaneous preferences for animacy signals, such as certain kinds of motion or a face-like appearance. Imprinting is used as a behavioural paradigm for studies on memory formation, early learning and predispositions, as well as number and space cognition, and brain asymmetries. Here, we present an automatized setup to expose and/or test animals for a variety of imprinting experiments. The setup consists of a cage with two high-frequency screens at the opposite ends where stimuli are shown. Provided with a camera covering the whole space of the cage, the behaviour of the animal is recorded continuously. A graphic user interface implemented in Matlab allows a custom configuration of the experimental protocol, that together with Psychtoolbox drives the presentation of images on the screens, with accurate time scheduling and a highly precise framerate. The setup can be implemented into a complete workflow to analyse behaviour in a fully automatized way by combining Matlab (and Psychtoolbox) to control the monitor screens and stimuli, DeepLabCut to track animals' behaviour, Python (and R) to extract data and perform statistical analyses. The automated setup allows neuro-behavioural scientists to perform standardized protocols during their experiments, with faster data collection and analyses, and reproducible results.
Identifiants
pubmed: 34272970
doi: 10.1007/s00422-021-00886-6
pii: 10.1007/s00422-021-00886-6
pmc: PMC8642325
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
575-584Informations de copyright
© 2021. The Author(s).
Références
Anderson DJ, Perona P (2014) Toward a science of computational ethology. Neuron 84(1):18–31. https://doi.org/10.1016/j.neuron.2014.09.005
doi: 10.1016/j.neuron.2014.09.005
pubmed: 25277452
Andrew RJ (1991) Neural and behavioural plasticity: the use of the domestic chick as a model. Oxford University Press
doi: 10.1093/acprof:oso/9780198521846.001.0001
Bateson PPG (1974) The characteristics and context of imprinting. In: William BD, Van der Kloot G, Walcott C (eds) Readings in behavior. Ardent Media, p 792
Bolhuis JJ (1991) Mechanisms of avian imprinting. Biol Rev Camb Philos Soc 66(4):303–345. https://doi.org/10.1111/j.1469-185X.1991.tb01145.x
doi: 10.1111/j.1469-185X.1991.tb01145.x
pubmed: 1801945
Bolhuis JJ, Honey RC (1998) Imprinting, learning and development: from behaviour to brain and back. Trends Neurosci 306(7):306–311
doi: 10.1016/S0166-2236(98)01258-2
Brainard DH (1997) The psychophsycis toolbox. Spat vis 10(4):433–436
doi: 10.1163/156856897X00357
Chiandetti C, Vallortigara G (2018) Chicken—cognition in the poultry yard. In: Bueno-Guerra N, Amici F (eds) Field and laboratory methods in animal cognition: a comparative guide. Cambridge University Press
De Margerie E, Lumineau S, Houdelier C, Richard Yris MA (2011) Influence of a mobile robot on the spatial behaviour of quail chicks. Bioinspir Biomim. https://doi.org/10.1088/1748-3182/6/3/034001
doi: 10.1088/1748-3182/6/3/034001
pubmed: 21869465
Gribovskiy A, Mondada F, Deneubourg JL, Cazenille L, Bredeche N, Halloy J (2015) Automated analysis of behavioural variability and filial imprinting of chicks (G. gallus), using autonomous robots, pp 1–17. http://arxiv.org/abs/1509.01957
Hess EH (1959) Imprinting. Science 130(3368):133–141
doi: 10.1126/science.130.3368.133
Horn G (1985) Memory, imprinting, and the brain: an inquiry into mechanisms. Oxford University Press
doi: 10.1093/acprof:oso/9780198521563.001.0001
Horn G (1998) Visual imprinting and the neural mechanisms of recognition memory. Trends Neurosci 21(7):300–305. https://doi.org/10.1016/S0166-2236(97)01219-8
doi: 10.1016/S0166-2236(97)01219-8
pubmed: 9683322
Inger R, Bennie J, Davies TW, Gaston KJ (2014) Potential biological and ecological effects of flickering artificial light. PLoS ONE. https://doi.org/10.1371/journal.pone.0098631
doi: 10.1371/journal.pone.0098631
pubmed: 25250775
pmcid: 4175084
Izawa E-I, Yanagihara S, Atsumi T, Matsushima T (2001) The role of basal ganglia in reinforcement learning and imprinting in domestic chicks. NeuroReport 12(8):1743–1747
doi: 10.1097/00001756-200106130-00045
Jackson C, McCabe BJ, Nicol AU, Grout AS, Brown MW, Horn G (2008) Dynamics of a memory trace: effects of sleep on consolidation. Curr Biol 18(6):393–400. https://doi.org/10.1016/j.cub.2008.01.062
doi: 10.1016/j.cub.2008.01.062
pubmed: 18356057
Johansson G (1973) Visual perception of biological motion and a model for its analysis. Percept Psychophys 14(2):201–211. https://doi.org/10.3758/BF03212378
doi: 10.3758/BF03212378
Jolly L, Pittet F, Caudal JP, Mouret JB, Houdelier C, Lumineau S, De Margerie E (2016) Animal-to-robot social attachment: Initial requisites in a gallinaceous bird. Bioinspir Biomim 11:1. https://doi.org/10.1088/1748-3190/11/1/016007
doi: 10.1088/1748-3190/11/1/016007
Josserand M, Lemaire BS (2020) A step by step guide to using visual field analysis. Protocols. https://doi.org/10.17504/protocols.io.bicvkaw6
doi: 10.17504/protocols.io.bicvkaw6
Josserand M, Rosa-Salva O, Versace E, Lemaire B (2021) Visual field analysis: a reliable method to score left- and right eye-use using automated tracking. https://doi.org/10.1101/2021.05.08.443242
Kim C, Ruberto T, Phamduy P, Porfiri M (2018) Closed-loop control of zebrafish behaviour in three dimensions using a robotic stimulus. Sci Rep 8(1):1–15. https://doi.org/10.1038/s41598-017-19083-2
doi: 10.1038/s41598-017-19083-2
Labuguen R, Matsumoto J, Negrete SB, Nishimaru H, Nishijo H, Takada M, Go Y, Inoue KI, Shibata T (2021) MacaquePose: a novel, “In the Wild” Macaque Monkey Pose Dataset for Markerless Motion Capture. Front Behav Neurosci 14:5. https://doi.org/10.3389/fnbeh.2020.581154
doi: 10.3389/fnbeh.2020.581154
Landgraf T, Bierbach D, Nguyen H, Muggelberg N, Romanczuk P, Krause J (2016) RoboFish: increased acceptance of interactive robotic fish with realistic eyes and natural motion patterns by live Trinidadian guppies. Bioinspir Biomimetics 11:1. https://doi.org/10.1088/1748-3190/11/1/015001
doi: 10.1088/1748-3190/11/1/015001
Leibovich T, Katzin N, Harel M, Henik A (2017) From “sense of number” to “sense of magnitude”: the role of continuous magnitudes in numerical cognition. Behav Brain Sci. https://doi.org/10.1017/S0140525X16000960
doi: 10.1017/S0140525X16000960
pubmed: 29342648
Lemaire BS, Rugani R, Regolin L, Vallortigara G (2020) Response of male and female domestic chicks to change in the number (quantity) of imprinting objects. Learn Behav 49(1):54–66. https://doi.org/10.3758/s13420-020-00446-1
doi: 10.3758/s13420-020-00446-1
pubmed: 33025570
pmcid: 7979580
Lemaire BS, Rucco D, Josserand M, Vallortigara G, Versace E (2021) Stability and individual variability of social attachment in imprinting. Sci Rep 11(1):1–12. https://doi.org/10.1038/s41598-021-86989-3
doi: 10.1038/s41598-021-86989-3
Lisney TJ, Rubene D, Rózsa J, Løvlie H, Håstad O, Ödeen A (2011) Behavioural assessment of flicker fusion frequency in chicken Gallus gallus domesticus. Vis Res 51(12):1324–1332. https://doi.org/10.1016/j.visres.2011.04.009
doi: 10.1016/j.visres.2011.04.009
pubmed: 21527269
Lisney TJ, Ekesten B, Tauson R, Håstad O, Ödeen A (2012) Using electroretinograms to assess flicker fusion frequency in domestic hens Gallus gallus domesticus. Vis Res 62:125–133. https://doi.org/10.1016/j.visres.2012.04.002
doi: 10.1016/j.visres.2012.04.002
pubmed: 22521657
Lorenz KZ (1937) The companion in the bird’s. World 54(3):245–273
Lorenzi E, Perrino M, Vallortigara G (2021) Numerosities and other magnitudes in the brains: a comparative view. Front Psychol 12(April):1–16. https://doi.org/10.3389/fpsyg.2021.641994
doi: 10.3389/fpsyg.2021.641994
Marino L (2017) Thinking chickens: a review of cognition, emotion, and behavior in the domestic chicken. Anim Cogn 20(2):127–147. https://doi.org/10.1007/s10071-016-1064-4
doi: 10.1007/s10071-016-1064-4
pubmed: 28044197
pmcid: 5306232
Martinho AI, Kacelnik A (2017) Ducklings imprint on the relational concept of “same or different.” Science 355(6327):286–289. https://doi.org/10.1126/science.aai7431
doi: 10.1126/science.aai7431
Mathis A, Mamidanna P, Cury KM, Abe T, Murthy VN, Mathis MW, Bethge M (2018) DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat Neurosci 21(9):1281–1289. https://doi.org/10.1038/s41593-018-0209-y
doi: 10.1038/s41593-018-0209-y
pubmed: 30127430
Mccabe BJ (2013) Imprinting. Wiley Interdiscip Rev Cogn Sci 4(4):375–390. https://doi.org/10.1002/wcs.1231
doi: 10.1002/wcs.1231
pubmed: 26304225
McCabe BJ (2019) Visual imprinting in birds: behavior, models, and neural mechanisms. Front Physiol 10:4. https://doi.org/10.3389/fphys.2019.00658
doi: 10.3389/fphys.2019.00658
Miura M, Matsushima T (2012) Preference for biological motion in domestic chicks: sex-dependent effect of early visual experience. Anim Cogn 15(5):871–879. https://doi.org/10.1007/s10071-012-0514-x
doi: 10.1007/s10071-012-0514-x
pubmed: 22622813
Miura M, Matsushima T (2016) Biological motion facilitates filial imprinting. Anim Behav 116:171–180. https://doi.org/10.1016/j.anbehav.2016.03.025
doi: 10.1016/j.anbehav.2016.03.025
Miura M, Nishi D, Matsushima T (2020) Combined predisposed preferences for colour and biological motion make robust development of social attachment through imprinting. Anim Cogn 23(1):169–188. https://doi.org/10.1007/s10071-019-01327-5
doi: 10.1007/s10071-019-01327-5
pubmed: 31712936
Nakamori T, Maekawa F, Sato K, Tanaka K, Ohki-Hamazaki H (2013) Neural basis of imprinting behavior in chicks. Dev Growth Differ 55(1):198–206. https://doi.org/10.1111/dgd.12028
doi: 10.1111/dgd.12028
pubmed: 23294362
Nath T, Mathis A, Chen AC, Patel A, Bethge M, Mathis MW (2019) Using DeepLabCut for 3D markerless pose estimation across species and behaviors. Nat Protoc 14(7):2152–2176. https://doi.org/10.1038/s41596-019-0176-0
doi: 10.1038/s41596-019-0176-0
pubmed: 31227823
Pelli DG (1997) The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat vis 26(10):437–442
doi: 10.1163/156856897X00366
Polverino G, Abaid N, Kopman V, MacRì S, Porfiri M (2012) Zebrafish response to robotic fish: preference experiments on isolated individuals and small shoals. Bioinspir Biomim 7:3. https://doi.org/10.1088/1748-3182/7/3/036019
doi: 10.1088/1748-3182/7/3/036019
Polverino G, Phamduy P, Porfiri M (2013) Fish and robots swimming together in a water tunnel: robot color and tail-beat frequency influence fish behavior. PLoS ONE 8(10):47–50. https://doi.org/10.1371/journal.pone.0077589
doi: 10.1371/journal.pone.0077589
Regolin L, Vallortigara G, Zanforlin M (1995) Object and spatial representations in detour problems by chicks. Anim Behav 49(1):195–199. https://doi.org/10.1016/0003-3472(95)80167-7
doi: 10.1016/0003-3472(95)80167-7
Romano D, Stefanini C (2021) Unveiling social distancing mechanisms via a fish-robot hybrid interaction. Biol Cybern Reluga. https://doi.org/10.1007/s00422-021-00867-9
doi: 10.1007/s00422-021-00867-9
Romano D, Donati E, Benelli G, Stefanini C (2019) A review on animal–robot interaction: from bio-hybrid organisms to mixed societies. Biol Cybern 113(3):201–225. https://doi.org/10.1007/s00422-018-0787-5
doi: 10.1007/s00422-018-0787-5
pubmed: 30430234
Romano D, Benelli G, Stefanini C (2021) Opposite valence social information provided by bio-robotic demonstrators shapes selection processes in the green bottle fly. J R Soc Interface. https://doi.org/10.1098/rsif.2021.0056
doi: 10.1098/rsif.2021.0056
pubmed: 33726543
Rosa-Salva O, Regolin L, Vallortigara G (2010) Faces are special for newly hatched chicks: evidence for inborn domain-specific mechanisms underlying spontaneous preferences for face-like stimuli. Dev Sci 13(4):565–577. https://doi.org/10.1111/j.1467-7687.2009.00914.x
doi: 10.1111/j.1467-7687.2009.00914.x
pubmed: 20590721
Rosa Salva O, Mayer U, Vallortigara G (2015) Roots of a social brain: developmental models of emerging animacy-detection mechanisms. Neurosci Biobehav Rev 50:150–168. https://doi.org/10.1016/j.neubiorev.2014.12.015
doi: 10.1016/j.neubiorev.2014.12.015
pubmed: 25544151
Rosa-Salva O, Grassi M, Lorenzi E, Regolin L, Vallortigara G (2016) Spontaneous preference for visual cues of animacy in naïve domestic chicks: the case of speed changes. Cognition 157:49–60. https://doi.org/10.1016/j.cognition.2016.08.014
doi: 10.1016/j.cognition.2016.08.014
pubmed: 27592411
Rosa-Salva O, Hernik M, Broseghini A, Vallortigara G (2018) Visually-naïve chicks prefer agents that move as if constrained by a bilateral body-plan. Cognition 173:106–114. https://doi.org/10.1016/j.cognition.2018.01.004
doi: 10.1016/j.cognition.2018.01.004
pubmed: 29367016
Rosa-Salva O, Mayer U, Versace E, Hébert M, Lemaire BS, Vallortigara G (2021) Sensitive periods for social development: interactions between predisposed and learned mechanisms. Cognition 5:4. https://doi.org/10.1016/j.cognition.2020.104552
doi: 10.1016/j.cognition.2020.104552
Rose SPR (2000) God’s organism? The chick as a model system for memory studies. Learn Mem 7(1):1–17. https://doi.org/10.1101/lm.7.1.1
doi: 10.1101/lm.7.1.1
pubmed: 10706598
Rugani R, Fontanari L, Simoni E, Regolin L, Vallortigara G (2009) Arithmetic in newborn chicks. Proc R Soc B Biol Sci 276(1666):2451–2460. https://doi.org/10.1098/rspb.2009.0044
doi: 10.1098/rspb.2009.0044
Rugani R, Regolin L, Vallortigara G (2010) Imprinted numbers: newborn chicks’ sensitivity to number vs continuous extent of objects they have been reared with. Dev Sci 13(5):790–797. https://doi.org/10.1111/j.1467-7687.2009.00936.x
doi: 10.1111/j.1467-7687.2009.00936.x
pubmed: 20712745
Rugani R, Regolin L, Vallortigara G (2011) Summation of large numerousness by newborn chicks. Front Psychol 2:1–8. https://doi.org/10.3389/fpsyg.2011.00179
doi: 10.3389/fpsyg.2011.00179
Rugani R, Cavazzana A, Vallortigara G, Regolin L (2013) One, two, three, four, or is there something more? Numerical discrimination in day-old domestic chicks. Anim Cogn 16(4):557–564. https://doi.org/10.1007/s10071-012-0593-8
doi: 10.1007/s10071-012-0593-8
pubmed: 23334508
Rugani R, Loconsole M, Regolin L (2017) A strategy to improve arithmetical performance in four day-old domestic chicks (Gallus gallus). Sci Rep 7(1):1–7. https://doi.org/10.1038/s41598-017-13677-6
doi: 10.1038/s41598-017-13677-6
Santolin C, Rosa-Salva O, Lemaire BS, Regolin L, Vallortigara G (2020) Statistical learning in domestic chicks is modulated by strain and sex. Sci Rep 10(1):1–8. https://doi.org/10.1038/s41598-020-72090-8
doi: 10.1038/s41598-020-72090-8
Spalding DA (1873) Instinct with original observations on young animals. Macmillan Mag 27:282–293
Vallortigara G (2012) The cognitive chicken: visual and spatial cognition in a non-mammalian brain. In: Zentall TR, Wasserman EA (eds) The Oxford handbook of comparative cognition. Oxford University Press, pp 48–66
Vallortigara G (2015) Foundations of number and space representations in non-human species. In: Evolutionary origins and early development of number processing, 1st edn, vol 1. Elsevier Inc. https://doi.org/10.1016/b978-0-12-420133-0.00002-8
Vallortigara G (2021) Born knowing. The origins of knowledge. MIT press
Vallortigara G, Regolin L (2006) Gravity bias in the interpretation of biological motion by inexperienced chicks. Curr Biol 16(8):279–280. https://doi.org/10.1016/j.cub.2006.03.052
doi: 10.1016/j.cub.2006.03.052
Vallortigara G, Versace E (2018) Filial imprinting. In: Vonk J, Shackelford TK (eds) Encyclopedia of animal cognition and behavior. Springer, Berlin
Vallortigara G, Regolin L, Rigoni M, Zanforlin M (1998) Delayed search for a concealed imprinted object in the domestic chick. Anim Cogn 1(1):17–24. https://doi.org/10.1007/s100710050003
doi: 10.1007/s100710050003
Vallortigara G, Regolin L, Marconato F (2005) Visually inexperienced chicks exhibit spontaneous preference for biological motion patterns. PLoS Biol 3(7):1312–1316. https://doi.org/10.1371/journal.pbio.0030208
doi: 10.1371/journal.pbio.0030208
Vallortigara G, Regolin L, Chiandetti C, Rugani R (2010) Rudiments of mind: insights through the chick model on number and space cognition in animals. Comp Cogn Behav Rev 5:78–99. https://doi.org/10.3819/ccbr.2010.50004
doi: 10.3819/ccbr.2010.50004
Versace E, Vallortigara G (2015) Origins of knowledge: insights from precocial species. Front Behav Neurosci 9:1–10. https://doi.org/10.3389/fnbeh.2015.00338
doi: 10.3389/fnbeh.2015.00338
Versace E, Schill J, Nencini AM, Vallortigara G (2016) Naïve chicks prefer hollow objects. PLoS ONE 11(11):1–16. https://doi.org/10.1371/journal.pone.0166425
doi: 10.1371/journal.pone.0166425
Versace E, Spierings MJ, Caffini M, ten Cate C, Vallortigara G (2017) Spontaneous generalization of abstract multimodal patterns in young domestic chicks. Anim Cogn 20(3):521–529. https://doi.org/10.1007/s10071-017-1079-5
doi: 10.1007/s10071-017-1079-5
pubmed: 28260155
Versace E, Martinho-Truswell A, Kacelnik A, Vallortigara G (2018) Priors in animal and artificial intelligence: where does learning begin? Trends Cogn Sci 22(11):963–965. https://doi.org/10.1016/j.tics.2018.07.005
doi: 10.1016/j.tics.2018.07.005
pubmed: 30097305
Wood JN (2013) Newborn chickens generate invariant object representations at the onset of visual object experience. Proc Natl Acad Sci USA 110(34):14000–14005. https://doi.org/10.1073/pnas.1308246110
doi: 10.1073/pnas.1308246110
pubmed: 23918372
pmcid: 3752245
Wood JN (2017) Spontaneous preference for slowly moving objects in visually Naïve animals. Open Mind 1(2):111–122. https://doi.org/10.1162/opmi_a_00012
doi: 10.1162/opmi_a_00012
Wood SMW, Wood JN (2015) Face recognition in newly hatched chicks at the onset of vision. J Exp Psychol Anim Learn Cogn 41(2):206–215. https://doi.org/10.1037/xan0000059
doi: 10.1037/xan0000059
pubmed: 25867056
Worley NB, Djerdjaj A, Christianson JP (2019) Convolutional neural network analysis of social novelty preference using DeepLabCut. BioRxiv. https://doi.org/10.1101/736983
doi: 10.1101/736983
Wu JJS, Hung A, Lin YC, Chiao CC (2020) Visual attack on the moving prey by Cuttlefish. Front Physiol 11(June):1–11. https://doi.org/10.3389/fphys.2020.00648
doi: 10.3389/fphys.2020.00648
Yamaguchi S, Aoki N, Kitajima T, Iikubo E, Katagiri S, Matsushima T, Homma KJ (2012) Thyroid hormone determines the start of the sensitive period of imprinting and primes later learning. Nat Commun 3:2–11. https://doi.org/10.1038/ncomms2088
doi: 10.1038/ncomms2088
Zanon M, Potrich D, Bortot M, Vallortigara G (2021) Towards a standardization of non-symbolic numerical experiments: GeNEsIS, a flexible and user-friendly tool to generate controlled stimuli. Behav Res Methods. https://doi.org/10.3758/s13428-021-01580-y
doi: 10.3758/s13428-021-01580-y
pubmed: 34117632