Combined predisposed preferences for colour and biological motion make robust development of social attachment through imprinting

  • Momoko Miura
  • Daisuke Nishi
  • Toshiya MatsushimaEmail author
Original Paper


To study how predisposed preferences shape the formation of social attachment through imprinting, newly hatched domestic chicks (Gallus gallus domesticus) were simultaneously exposed to two animations composed of comparable light points in different colours (red and yellow), one for a walking motion and another for a linear motion. When a walking animation in red was combined with a linear one in yellow, chicks formed a learned preference for the former that represented biological motion (BM). When the motion–colour association was swapped, chicks failed to form a preference for a walking in yellow, indicating a bias to a specific association of motion and colour. Accordingly, experiments using realistic walking chicken videos revealed a preference for a red video over a yellow one, when the whole body or the head was coloured. On the other hand, when the BM preference had been pre-induced using an artefact moving rigidly (non-BM), a clear preference for a yellow walking animation emerged after training by the swapped association. Even if the first-seen moving object was a nonbiological artefact such as the toy, the visual experience would induce a predisposed BM preference, making chicks selectively memorize the object with natural features. Imprinting causes a rapid inflow of thyroid hormone in the telencephalon leading to the induction of the BM preference, which would make the robust formation of social attachment selectively to the BM-associated object such as the mother hen.


Early social deprivation Sensitive period Thyroid hormone Developmental homeostasis Conspec–Conlern mechanism Domestic chicks 



We thank Dr. Giorgio Vallortigara (University of Trento, Italy) for his critical comments and discussions on our manuscript. We also thank the editor and anonymous referees for instructive suggestions. Contribution of Mr. Yasutaka Sasaki (Machine Department of the Faculty of Science, Hokkaido University) must be acknowledged for production of the imprinting apparatus.

Author contributions

TM and MM conceived the study and designed the experiments. MM developed the animations, designed the experimental procedures, analysed the data, and prepared the figures. MM and DN carried out the experiments. T.M. developed the apparatus and the computer programmes. TM and MM wrote the manuscript and supplementary materials. All the authors gave final approval for publication.


The present study was supported by grants funded to TM by the Japan Society for Promotion of Science (JSPS, Kakenhi; Grants-in-aid for Scientific Research #25291071, #26650114, #18K07351).

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  1. Aoki N, Yamaguchi S, Kitajima T, Takehara A, Katagiri-Nakagawa S, Matsui R, Watanabe D, Matsushima T, Homma KJ (2015) Critical role of the neural pathway from the intermediate medial mesopallium to the intermediate hyperpallium apicale in filial imprinting of domestic chicks (Gallus gallus domesticus). Neuroscience 308:115–124. CrossRefPubMedGoogle Scholar
  2. Barki A, Volpato GL (1998) Early social environment and the fighting behaviour of young Oreochromis niloticus (Pisces, Cichlidae). Behaviour 135:913–929CrossRefGoogle Scholar
  3. Bolhuis JJ (1999) Early learning and the development of filial preferences in the chick. Behav Brain Res 98:245–252. CrossRefPubMedGoogle Scholar
  4. Bolhuis JJ, Honey RC (1998) Imprinting, learning and development: from behaviour to brain and back. Trends Neurosci 21:306–311. CrossRefPubMedGoogle Scholar
  5. Bolhuis JJ, Johnson MH, Horn G (1985) Effects of early experience on the development of filial preferences in the domestic chick. Dev Psychobiol 18:299–308. CrossRefPubMedGoogle Scholar
  6. Buiatti M, Di Giorgio E, Piazza M, Menna G, Taddei F, Baldo E, Vallortigara G (2019) Proc Natl Acad Sci USA 116:4625–4630. CrossRefPubMedGoogle Scholar
  7. Carlson M, Earls F (1995) Psychological and neuroendocrinological sequelae of early social deprivation in institutionalized children in Romania. Ann N Y Acad Sci 807:419–428. CrossRefGoogle Scholar
  8. Casile A, Giese MA (2006) Nonvisual motor training influences biological motion perception. Curr Biol 16:69–74. CrossRefPubMedGoogle Scholar
  9. Csillag A (1999) Striato-telencephalic and striato-tegmental circuits: relevance to learning in domestic chicks. Behav Brain Res 98:227–236. CrossRefPubMedGoogle Scholar
  10. Daisley JN, Vallortigara G, Regolin L (2010) Logic in an asymmetrical (social) brain: transitive inference in the young domestic chick. Soc Neurosci 5:309–319. CrossRefPubMedGoogle Scholar
  11. Di Giorgio E, Loveland JL, Mayer U, Rosa-Salva O, Versace E, Vallortigara G (2017) Filial responses as predisposed and learned preferences: early attachment in chicks and babies. Behav Brain Res 325:90–104. CrossRefPubMedGoogle Scholar
  12. Harlow HF, Suomi SJ (1971) Social recovery by isolation-reared monkeys. Proc Natl Acad Sci USA 68:1534–1538. CrossRefPubMedGoogle Scholar
  13. Harlow HF, Dodsworth RO, Harlow MK (1965) Total social isolation in monkeys. Proc Natl Acad Sci USA 54:90–97. CrossRefPubMedGoogle Scholar
  14. Hess EH (1958) “Imprinting” in animals. Sci Am 198:81–90CrossRefGoogle Scholar
  15. Hogue ME, Beaugrand JP, Laguë PC (1996) Coherent use of information by hens observing their former dominant defeating or being defeated by a stranger. Behav Proc 38:241–252. CrossRefGoogle Scholar
  16. Horn G (1985) Memory, imprinting and the brain, an inquiry into mechanisms. Oxford University Press, OxfordCrossRefGoogle Scholar
  17. Horn G (1998) Visual imprinting and the neural mechanisms of recognition memory. Trends Neurosci 21:300–305. CrossRefPubMedGoogle Scholar
  18. Horn G (2004) Pathways of the past: the imprint of memory. Nat Rev Neurosci 5:108–120. CrossRefPubMedGoogle Scholar
  19. Ichihashi T, Ichikawa Y, Matsushima T (2004) A non-social and isolate rearing condition induces an irreversible shift toward continued fights in the male fighting fish (Betta splendens). Zool Sci 21:723–729. CrossRefPubMedGoogle Scholar
  20. Izawa EI, Yanagihara S, Atsumi T, Matsushima T (2001) The role of basal ganglia in reinforcement learning and imprinting in domestic chicks. NeuroReport 12:1743–1747. CrossRefPubMedGoogle Scholar
  21. Johansson G (1973) Visual perception of biological motion and a model for its analysis. Percept Psychophys 14:201–211. CrossRefGoogle Scholar
  22. Johnson MH, Horn G (1988) Development of filial preferences in dark-reared chicks. Anim Behav 36:675–683. CrossRefGoogle Scholar
  23. Johnson MH, Bolhuis JJ, Horn G (1985) Interaction between acquired preferences and developing predispositions during imprinting. Anim Behav 33:1000–1006. CrossRefGoogle Scholar
  24. Johnson MH, Davies DC, Horn G (1989) A sensitive period for the development of a predisposition in dark-reared chicks. Anim Behav 37:1044–1046CrossRefGoogle Scholar
  25. Lee SA, Spelke ES, Vallortigara G (2012) Chicks, like children, spontaneously reorient by three-dimensional environmental geometry, not by image matching. Biol Lett 8:492–494. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lorenz K (1937) The companion in the bird’s world. Auk 54:245–273. CrossRefGoogle Scholar
  27. Lorenzi E, Mayer U, Rosa-Salva O, Vallortigara G (2017) Dynamic features of animate motion activate septal and preoptic areas in visually naïve chicks (Gallus gallus). Neuroscience 354:54–68. CrossRefPubMedGoogle Scholar
  28. Lorenzi E, Pross A, Rosa-Salva O, Versace E, Sgadò P, Vallortigara G (2019) Embryonic exposure to valproic acid affects social predispositions for dynamic cues of animate motion in newly-hatched chicks. Front Physiol 10:501. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Maekawa F, Komine O, Sato K, Kanamatsu T, Uchiyama M, Tanaka K, Ohki-Hamazaki H (2006) Imprinting modulates processing of visual information in the visual wulst of chicks. BMC Neurosci 7:75. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Makinodan M, Rosen KM, Ito S, Corfas G (2012) A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science 337:1357–1360. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Martinho A III, Kacelnik A (2016) Ducklings imprint on the relational concept of “same or different”. Science 353:286–288. CrossRefPubMedGoogle Scholar
  32. Mascalzoni E, Regolin L, Vallortigara G (2010) Innate sensitivity for self-propelled causal agency in newly hatched chicks. Proc Natl Acad Sci USA 107:4483–4485. CrossRefPubMedGoogle Scholar
  33. Matsushima T, Izawa EI, Aoki N, Yanagihara S (2003) The mind through chick eyes: memory, cognition and anticipation. Zool Sci 20:395–408. CrossRefPubMedGoogle Scholar
  34. Maurer D, Barrera M (1981) Infants’ perception of natural and distorted arrangements o f a schematic face. Child Dev 47:523–527. CrossRefGoogle Scholar
  35. Mayer U, Rosa-Salva O, Vallortigara G (2017a) First exposure to an alive conspecific activates septal and amygdaloid nuclei in visually-naïve domestic chicks (Gallus gallus). Behav Brain Res 317:71–81. CrossRefPubMedGoogle Scholar
  36. Mayer U, Rosa-Salva O, Morbioli F, Vallortigara G (2017b) The motion of a living conspecific activates septal and preoptic areas in naive domestic chicks (Gallus gallus). Eur J Neurosci 45:423–432. CrossRefPubMedGoogle Scholar
  37. Miura M, Matsushima T (2012) Preference for biological motion in domestic chicks: sex-dependent effect of early visual experience. Anim Cogn 15:871–879. CrossRefPubMedGoogle Scholar
  38. Miura M, Matsushima T (2016) Biological motion facilitates filial imprinting. Anim Behav 116:171–180. CrossRefGoogle Scholar
  39. Miura M, Aoki N, Yamaguchi S, Homma KJ, Matsushima T (2018) Thyroid hormone sensitizes the imprinting-associated induction of biological motion preference in domestic chicks. Front Physiol 9:1740. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Mondloch CJ, Lewis TL, Budreau DR, Maurer D, Dannemiller JL, Stephens BR, Kleiner-Gathercoal KA (1999) Face perception during early infancy. Psychol Sci 10:419–422. CrossRefGoogle Scholar
  41. Morton J, Johnson MH (1991) Conspec and Conlern: a two-process theory of infant face recognition. Psychol Rev 98:164–181. CrossRefPubMedGoogle Scholar
  42. Moulson MC, Shutts K, Fox NA, Zeahah CH, Spelke ES, Nelson CA (2015) Effects of early institutionalization on the development of emotion processing: a case for relative sparing? Dev Sci 18:298–313. CrossRefPubMedGoogle Scholar
  43. Naumova OY, Rychkov SY, Kornilov SA, Odintsova VV, Anikina VO, Solodunova MY, Arintcina IA, Zhukova MA, Ovchinnikova IV, Burenkova OV, Zhukova OV, Muhamedrahimov RJ, Grigorenko EL (2019) Effects of early social deprivation on epigenetic statuses and adaptive behavior of young children: a study based on a cohort of institutionalized infants and toddlers. PLoS One 14:e0214285. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Nishigori H, Kagami K, Takahashi A, Tezuka Y, Sanbe A, Nishigori H (2013) Impaired social behavior in chicks exposed to sodium valproate during the last week of embryogenesis. Psychopharmacology 227:393–402. CrossRefPubMedGoogle Scholar
  45. Pecchia T, Vallortigara G (2010) View-based strategy for reorientation by geometry. J Exp Biol 213:2987–2996. CrossRefPubMedGoogle Scholar
  46. Pecchia T, Vallortigara G (2012) Spatial reorientation by geometry with freestanding objects and extended surfaces: a unifying view. Proc R Soc B 279:2228–2236. CrossRefPubMedGoogle Scholar
  47. Reid VM, Dunn K, Young RJ, Amu J, Donovan T, Reissland N (2017) The human fetus preferentially engages with face-like visual stimuli. Curr Biol 27:1825–1828. CrossRefPubMedGoogle Scholar
  48. 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 13:565–577. CrossRefPubMedGoogle Scholar
  49. Rosa-Salva O, Mayer U, Vallortigara G (2015) Roots of a social brain: developmental models of emerging animacy-detection mechanisms. Neurosci Biobehav Rev 50:150–1168. CrossRefPubMedGoogle Scholar
  50. 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. CrossRefPubMedGoogle Scholar
  51. Rugani R, Fontanari L, Simoni E, Regolin L, Vallortigara G (2009) Arithmetic in newborn chicks. Proc R Soc B 276:2451–2460. CrossRefPubMedGoogle Scholar
  52. 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 16:557–564. CrossRefPubMedGoogle Scholar
  53. Rugani R, Vallortigara G, Priftis K, Regolin L (2015) Number-space mapping in the newborn chick resembles humans’ mental number line. Science 347:534–536. CrossRefPubMedGoogle Scholar
  54. Santolin C, Rosa-Salva O, Vallortigara G, Regolin L (2016) Unsupervised statistical learning in newly hatched chicks. Curr Biol 26:1218–1220. CrossRefGoogle Scholar
  55. Sgadò P, Rosa-Salva O, Versace E, Vallortigara G (2018) Embryonic exposure to valproic acid impairs social predispositions of newly-hatched chicks. Sci Rep 8:5919. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Simion F, Regolin L, Bulf H (2008) A predisposition for biological motion in the newborn baby. Proc Natl Acad Sci USA 105:809–813. CrossRefPubMedGoogle Scholar
  57. Sluckin W (1964) Imprinting and early learning: page 26 (chapter 2, “approach and following responses”; section 2, “moving objects”). Spottiswoode, Ballantyne & Co. Ltd., LondonGoogle Scholar
  58. Spalding D (1873) Instinct with original observations on young animals. Macmillan’s Mag 27:282–293 (Reprinted in British Journal of Animal Behaviour 2:2–11 in 1954) Google Scholar
  59. Spelke ES (2000) Core knowledge. Am Psychol 55:1233–1243. CrossRefPubMedGoogle Scholar
  60. Spelke ES, Kinzler KD (2007) Core knowledge. Dev Sci 10:89–96. CrossRefPubMedGoogle Scholar
  61. Sugita Y (2008) Face perception in monkeys reared with no exposure to faces. Proc Natl Acad Sci USA 105:394–398. CrossRefPubMedGoogle Scholar
  62. Takemura Y, Yamaguchi S, Aoki N, Miura M, Homma KJ, Matsushima T (2018) Gene expression of Dio2 (thyroid hormone converting enzyme) in telencephalon is linked with predisposed biological motion preference in domestic chicks. Behav Brain Res 349:25–30. CrossRefPubMedGoogle Scholar
  63. Tooker CP, Miller RJ (1980) The ontogeny of agonistic behaviour in the blue gourami, Trichogaster trichopterus (Pisces, Anabantoidei). Anim Behav 28:973–988. CrossRefGoogle Scholar
  64. Tóth M, Halász J, Mikics É, Barsy B, Haller J (2008) Early social deprivation induces disturbed social communication and violent aggression in adulthood. Behav Neurosci 122:849–854. CrossRefPubMedGoogle Scholar
  65. Vallortigara G (2012) Core knowledge of object, number, and geometry: a comparative and neural approach. Cognit Neuropsychol 29:213–236. CrossRefGoogle Scholar
  66. Vallortigara G, Regolin L (2006) Gravity bias in the interpretation of biological motion by inexperienced chicks. Curr Biol 16:279–280. CrossRefGoogle Scholar
  67. Vallortigara G, Regolin L, Marconato F (2005) Visually inexperienced chicks exhibit spontaneous preference for biological motion patterns. PLoS Biol 3:1312–1316. CrossRefGoogle Scholar
  68. Versace R, Schill J, Nencini AM, Vallortigara G (2016) Naïve chicks prefer hollow objects. PLoS One 11:e0166425. CrossRefPubMedPubMedCentralGoogle Scholar
  69. Versace E, Fracasso I, Baldan G, Della Zotte A, Vallortigara G (2017a) Newborn chicks show inherited variability in early social predispositions for hen-like stimuli. Sci Rep 7:40296. CrossRefPubMedPubMedCentralGoogle Scholar
  70. Versace E, Spierings MJ, Caffini M, ten Cate C, Vallortigara G (2017b) Spontaneous generalization of abstract multimodal patterns in young domestic chicks. Anim Cogn 20:521–529. CrossRefPubMedGoogle Scholar
  71. Versace E, Martinho-Truswel A, Kacelnik A, Vallortigara G (2018) Priors in animal and artificial intelligence: where does learning begin? Trends Cogn Sci 22:963–965. CrossRefPubMedGoogle Scholar
  72. Versace E, Ragusa M, Vallortigara G (2019) A transient time window for early predispositions in newborn chicks. bioRxiv. CrossRefGoogle Scholar
  73. Wood SMW, Wood JN (2015) A chicken model for studying the emergence of invariant object recognition. Front Neural Circuits 9:7. CrossRefPubMedPubMedCentralGoogle Scholar
  74. Xin Q, Ogura Y, Uno L, Matsushima T (2017) Selective contribution of the telencephalic arcopallium to the social facilitation of foraging efforts in the domestic chick. Eur J Neurosci 45:365–380. CrossRefPubMedGoogle Scholar
  75. 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 3:1081. CrossRefPubMedPubMedCentralGoogle Scholar
  76. Yamaguchi S, Aoki N, Matsushima T, Homma KJ (2018) Wnt-2b in the intermediate hyperpallium apicale of the telencephalon is critical for the thyroid hormone-mediated opening of the sensitive period for filial imprinting in domestic chicks (Gallus gallus domesticus). Horm Behav 102:120–128. CrossRefPubMedGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biology, Faculty of ScienceHokkaido UniversitySapporoJapan

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