Prenatal learning in an Australian songbird: Habituation and individual discrimination in superb fairy-wren embryos

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1797, 2014, Pages

  Colombelli Négrel, Diane ^a   Hauber, Mark E ^b   Kleindorfer, Sonia ^a  

^a FLINDERS UNIVERSITY   (Australia)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Embryonic learning; Malurus cyaneus; Prenatal discrimination; Songbirds

Indexed keywords

BEGGING BEHAVIOR; CONSPECIFIC; EMBRYONIC DEVELOPMENT; HABITUATION; HATCHING; INCUBATION; NEONATE; PARENT-OFFSPRING INTERACTION; PARENTAL CARE; SONGBIRD;

MALURUS CYANEUS; PASSERI; TROGLODYTINAE;

ANIMAL; AUDITORY STIMULATION; AUSTRALIA; EMBRYOLOGY; FEMALE; HABITUATION; HEART RATE; LEARNING; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; SONGBIRD; VOCALIZATION;

ACOUSTIC STIMULATION; ANIMALS; AUSTRALIA; DISCRIMINATION (PSYCHOLOGY); FEMALE; HABITUATION, PSYCHOPHYSIOLOGIC; HEART RATE; LEARNING; SONGBIRDS; VOCALIZATION, ANIMAL;

EID: 84908376955     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.1154     Document Type: Article

References (60)

1. Dukas R. 2013 Effects of learning on evolution: robustness, innovation and speciation. Anim. Behav. 278, 2705–2713.
2. Kleindorfer S, Hoi H, Evans C, Mahr K, Robertson J, Hauber ME, Colombelli-Négrel D. 2014 The cost of teaching embryos in superb fairy-wrens. Behav. Ecol. 25, 1131–1135. (doi:10.1093/beheco/aru097)
3. Kleindorfer S, Evans C, Colombelli-Négrel D. 2014 Females that experience threat are better teachers. Biol. Lett. 10, 20140046. (doi:10.1098/rsbl.2014.0046)
4. Goldstone RL, Son JY, Byrge L. 2011 Early perceptual learning. Infancy 16, 45–51. (doi:10. 1111/j.1532-7078.2010.00054.x)
5. Watanabe T, Náñez JE, Sasaki Y. 2001 Perceptual learning without perception. Nature 413, 844–848. (doi:10.1038/35101601)
6. Reed MS et al. 2010 What is social learning? Ecol. Soc. 15. See http://www.ecologyandsociety.org/ vol15/iss4/resp1/.
7. Wolpert DM, Diedrichsen J, Flanagan JR. 2011 Principles of sensorimotor learning. Nat. Rev. Neurosci. 12, 739–751. (doi:10.1038/nrn3112)
8. Chikahisa S et al. 2006 Exposure to music in the perinatal period enhances learning performance and alters BDNF/ TrkB signaling in mice as adults. Behav. Brain Res. 169, 312–319. (doi:10.1016/j.bbr.2006.01.021)
9. Kim H et al. 2006 Influence of prenatal noise and music on the spatial memory and neurogenesis in the hippocampus of developing rats. Brain Dev. 28, 109–114. (doi:10.1016/j.braindev.2005.05.008)
10. Moon C, Lagercrantz H, Kuhl PK. 2013 Language experienced in utero affects vowel perception after birth: a two-country study. Acta Paediatr. 102, 156–160. (doi:10.1111/apa.12098)
11. Sanyal T et al. 2013 Prenatal loud music and noise: differential impact on physiological arousal, hippocampal synaptogenesis and spatial behavior in one day-old chicks. PLoS ONE 8, e67347. (doi:10. 1371/journal.pone.0067347)
12. Wells DL, Hepper PG. 2006 Prenatal olfactory learning in the domestic dog. Anim. Behav. 72, 681–686. (doi:10.1016/j.anbehav.2005.12.008)
13. Hepper PG. 1988 Adaptive fetal learning: prenatal exposure to garlic affects postnatal preferences. Anim. Behav. 36, 935–936. (doi:10.1016/S0003- 3472(88)80177-5)
14. Lecanuet J-P, Granier-Deferre C, Jacquet A-Y, Busnel M-C. 1992 Decelerative cardiac responsiveness to acoustical stimulation in the near term fetus. Q. J. Exp. Psychol. B 44, 279–303.
15. Gottlieb G. 1979 Development of species identification in ducklings: V. Perceptual differentiation in the embryo. J. Comp. Physiol. Psychol. 93, 831–854. (doi:10.1037/h0077614)
16. Kisilevsky BS et al. 2003 Effects of experience on fetal voice recognition. Psychol. Sci. 14, 220–224. (doi:10.1111/1467-9280.02435)
17. Lecanuet JP, Granier-Deferre C, Jacquet AY, Capponi I, Ledru L. 1993 Prenatal discrimination of a male and a female voice uttering the same sentence. Early Dev. Parent. 2, 217–228. (doi:10.1002/edp.2430020405)
18. Lee C, Brown C, Hains S, Kisilevsky B. 2007 Fetal development: voice processing in normotensive and hypertensive pregnancies. Biol. Res. Nurs. 8, 272–282. (doi:10.1177/1099800406298448)
19. Caubet Y, Jaisson P, Lenoir A. 1992 Preimaginal induction of adult behaviour in insects. Q. J. Exp. Psychol. B 44, 165–178.
20. Hepper PG, Waldman B. 1992 Embryonic olfactory learning in frogs. Q. J. Exp. Psychol. B 44, 179–197.
21. Ferrari MC, Manek AK, Chivers DP. 2010 Temporal learning of predation risk by embryonic amphibians. Biol. Lett. 6, 308–310. (doi:10.1098/rsbl.2009.0798)
22. Darmaillacq A-S, Lesimple C, Dickel L. 2008 Embryonic visual learning in the cuttlefish, Sepia officinalis. Anim. Behav. 76, 131–134. (doi:10. 1016/j.anbehav.2008.02.006)
23. Sneddon H, Hadden R, Hepper PG. 1998 Chemosensory learning in the chicken embryo. Physiol. Behav. 64, 133–139. (doi:10.1016/S0031-9384(98)00037-7)
24. Kawai N. 2006 Cognitive abilities before birth: learning and long-lasting memory in a chimpanzee fetus. In Cognitive development in chimpanzees (eds T Matsuzawa, M Tomonaga, M Tanaka), pp. 48–63. New York, NY: Springer.
25. Kawai N, Morokuma S, Tomonaga M, Horimoto N, Tanaka M. 2004 Associative learning and memory in a chimpanzee fetus: learning and long-lasting memory before birth. Dev. Psychobiol. 44, 116–122. (doi:10.1002/dev.10160)
26. Bjorklund DF. 2009 Why youth is not wasted on the young: immaturity in human development. New York, NY: Wiley Press.
27. Colombelli-Négrel D et al. 2012 Embryonic learning of vocal passwords in superb fairy-wrens reveals intruder cuckoo nestlings. Curr. Biol. 22, 2155–2160. (doi:10.1016/j.cub.2012.09.025)
28. Lecanuet J-P. 1995 Fetal development: a psychobiological perspective. Erlbaum, NJ: Lawrence Erlbaum Associates, Inc.
29. Zimmer EZ et al. 1993 Response of the premature fetus to stimulation by speech sounds. Early Hum. Dev. 33, 207–215. (doi:10.1016/0378- 3782(93)90147-M)
30. Heaton MB, Galleher E. 1981 Prenatal auditory discrimination in the bobwhite quail. Behav. Neural. Biol. 31, 242–246. (doi:10.1016/S0163- 1047(81)91258-9)
31. Heaton MB. 1972 Prenatal auditory discrimination in the wood duck (Aix sponsa). Anim. Behav. 20, 421–424. (doi:10.1016/S0003-3472(72)80002-2)
32. Kisilevsky BS, Pang L, Hains SM. 2000 Maturation of human fetal responses to airborne sound in lowand high-risk fetuses. Early Hum. Dev. 58, 179–195. (doi:10.1016/S0378-3782(00)00075-X)
33. Kisilevsky BS, Hains SM. 2011 Onset and maturation of fetal heart rate response to the mother’s voice over late gestation. Dev. Sci. 14, 214–223. (doi:10. 1111/j.1467-7687.2010.00970.x)
34. Kisilevsky B et al. 2009 Fetal sensitivity to properties of maternal speech and language. Infant Behav. Dev. 32, 59–71. (doi:10.1016/j.infbeh.2008. 10.002)
35. Gottlieb G. 1988 Development of species identification in ducklings: XV. Individual auditory recognition. Dev. Psychobiol. 21, 509–522. (doi:10. 1002/dev.420210602)
36. Grier JB, Counter SA, Shearer WM. 1967 Prenatal auditory imprinting in chickens. Science 155, 1692–1693. (doi:10.1126/science.155.3770.1692)
37. Höchel J, Pirow R, Nichelmann M. 2002 Development of heart rate responses to acoustic stimuli in Muscovy duck embryos. Comp. Biochem. Physiol. A 131, 805–816. (doi:10.1016/S1095- 6433(02)00018-1)
38. Balaban E, Desco M, Vaquero JJ. 2012 Waking-like brain function in embryos. Curr. Biol. 22, 852–861. (doi:10.1016/j.cub.2012.03.030)
39. Darwin C. 1871 The descent of man and selection in relation to sex. London, UK: John Murray.
40. Doupe AJ, Kuhl PK. 1999 Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 22, 567–631. (doi:10.1146/annurev. neuro.22.1.567)
41. Kuhl PK. 2003 Human speech and birdsong: communication and the social brain. Proc. NatlAcad. Sci. USA 100, 9645–9646. (doi:10.1073/pnas. 1733998100)
42. Bolhuis JJ, Okanoya K, Scharff C. 2010 Twitter evolution: converging mechanisms in birdsong and human speech. Nat. Rev. Neurosci. 11, 747–759. (doi:10.1038/nrn2931)
43. Jarvis ED. 2006 Evolution of brain structures for vocal learning in birds: a synopsis. Acta Zool. Sinica 52, 85–89.
44. Jarvis ED. 2013 Evolution of brain pathways for vocal learning in birds and humans. In Birdsong, speech, and language: exploring the evolution of mind and brain (eds RC Berwick, N Chomsky, JJ Bolhuis, M Everaert), pp. 63–107. Cambridge, MA: MIT Press.
45. Lipkind D et al. 2013 Stepwise acquisition of vocal combinatorial capacity in songbirds and human infants. Nature 498, 104–108. (doi:10.1038/ nature12173)
46. Blumstein DT, Daniel JC. 2004 Yellow-bellied marmots discriminate between the alarm calls of individuals and are more responsive to calls from juveniles. Anim. Behav. 68, 1257–1265. (doi:10. 1016/j.anbehav.2003.12.024)
47. Colombelli-Négrel D, Gouat P. 2006 Male and female mound-building mice, Mus spicilegus, discriminate dietary and individual odours of conspecifics. Anim. Behav. 72, 577–583. (doi:10. 1016/j.anbehav.2005.11.015)
48. Hauber ME, Pearson HE, Reh A, Merges A. 2002 Discrimination between host songs by brood parasitic brown-headed cowbirds (Molothrus ater). Anim. Cogn. 5, 129–137. (doi:10.1007/s10071-002-0143-x)
49. Wetzel JM, Quigley KS, Morell J, Eves E, Backs RW. 2006 Cardiovascular measures of attention to illusory and nonillusory visual stimuli. J. Psychophysiol. 20, 276–285. (doi:10.1027/0269- 8803.20.4.276)
50. Courage ML, Reynolds GD, Richards JE. 2006 Infants’ attention to patterned stimuli: developmental change from 3 to 12 months of age. Child Dev. 77, 680–695. (doi:10.1111/j.1467-8624.2006.00897.x)
51. Lierz M, Gooss O, Hafez HM. 2006 Noninvasive heart rate measurement using a digital egg monitor in chicken and turkey embryos. J. Avian Med. Surg. 20, 141–146. (doi:10.1647/2005-017R.1)
52. Hauber ME, Russo SA, Sherman PW. 2001 A password for species recognition in a brood-parasitic bird. Proc. R. Soc. Lond. B 268, 1041–1048. (doi:10.1098/rspb.2001.1617)
53. Gentner TQ, Hulse SH, Bentley GE, Ball GF. 2000 Individual vocal recognition and the effect of partial lesions to HVc on discrimination, learning, and categorization of conspecific song in adult songbirds. J. Neurobiol. 42, 117–133. (doi:10.1002/(SICI)1097-4695(200001)42:1,117::AID-NEU11.3.0.CO;2-M)
54. Kazial KA, Kenny TL, Burnett SC. 2008 Little brown bats (Myotis lucifugus) recognize individual identity of conspecifics using sonar calls. Ethology 114, 469–478. (doi:10.1111/j.1439-0310.2008. 01483.x)
55. Bee MA, Gerhardt HC. 2002 Individual voice recognition in a territorial frog (Rana catesbeiana). Proc. R. Soc. Lond. B 269, 1443–1448. (doi:10. 1098/rspb.2002.2041)
56. Hare JF. 1998 Juvenile Richardson’s ground squirrels, Spermophilus richardsonii, discriminate among individual alarm callers. Anim. Behav. 55, 451–460. (doi:10.1006/anbe.1997.0613)
57. Langmore NE, Hunt S, Kilner RM. 2003 Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422, 157–160. (doi:10.1038/nature01460)
58. Ranjard L et al. 2010 Bioacoustic distances between the begging calls of brood parasites and their host species: a comparison of metrics and techniques. Behav. Ecol. Sociobiol. 64, 1915–1926. (doi:10. 1007/s00265-010-1065-2)
59. Langmore NE, Maurer G, Adcock GJ, Kilner RM. 2008 Socially acquired host-specific mimicry and the evolution of host races in Horsfield’s bronze-cuckoo Chalcites basalis. Evolution 62, 1689–1699. (doi:10. 1111/j.1558-5646.2008.00405.x)
60. Brenowitz EA, Beecher MD. 2005 Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci. 28, 127–132. (doi:10.1016/j.tins.2005.01.004)