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Organisational and Activational Effects of Prenatal Exposure to Testosterone on Lateralisation in the Domestic Chicken (Gallus gallus domesticus)

  • Bernd J. Riedstra
  • Kristina A. Pfannkuche
  • Antonius G. G. Groothuis
Chapter

Abstract

Brain lateralisation is the specialisation of the two hemispheres on different tasks and is supposedly beneficial for individuals. There is a long-standing debate about to what extent and via which pathways prenatal exposure to testosterone affects lateralisation. Birds are excellent models to investigate this since the embryo can be manipulated outside the mother’s body. Moreover, avian eggs contain substantial concentrations of maternally derived hormones known to affect a wide array of behaviours. Therefore, birds provide an excellent model to integrate two flourishing fields: that of hormone mediated maternal effects and of lateralisation. In addition, in most birds the eyes are placed laterally and the information exchange between the two hemispheres is limited, facilitating measuring lateralisation of visually guided behaviour. We will discuss results of egg injection experiments on short- and long-term effects on the lateralisation of visually guided behaviours in the domestic chicken. Lateralisation in young birds, young chicken in particular, has been extensively studied, but to what extent lateralisation is consistent over life and affected by prenatal exposure in adult birds remains elusive. Our results do not show an effect of the prenatal manipulation, in contrast to some other studies, perhaps because ours were carefully carried out within the physiological range of the species. They therefore do not lend support for either of the three main hypotheses about how prenatal testosterone affects the development of lateralisation in the ‘Geschwind-Behan–Galaburda’ hypothesis, the ‘Corpus Callosum’ hypothesis and the ‘sexual differentiation’ hypothesis. Correlations between testosterone levels and lateralisation both measured in adulthood suggest a role for activating effects of this hormone on lateralisation, at least in males. Correlations of lateralisation indices at young and adult age within individuals were also inconsistent, suggesting brain reorganisation during late development and challenging functional explanations of lateralisation for adult chickens.

Keywords

Corpus Callosum Sexual Differentiation Prenatal Exposure Adult Bird Tonic Immobility 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

GBG

The Geschwind-Behan–Galaburda hypothesis

T

Testosterone

CC

Corpus callosum

E2

Estradiol

SD

Sexual differentiation

Notes

Acknowledgments

We thank Mirte Greve, Sjoerd Veenstra, Roelie Veenstra-Wiegman, Bonnie de Vries, Ilse Weites, Martine Muller and Saskia Helder for their assistance during several phases of the current study. This experiment was conducted under licence number 4765A of the animal experimentation committee (DEC) from the University of Groningen. BR was funded by NWO-grant 051-14-016, KP by EU grant EDCBNL.

References

  1. Adret P, Rogers LJ (1989) Sex differences in the visual projections of young chicks: a quantitative study of the thalamofugal pathway. Brain Res 478:59–73PubMedCrossRefGoogle Scholar
  2. Balthazart J, Adkins-Regan EA (2003) Sexual differentiation of brain and behaviour in birds. In: Pfaff D, Arnold A, Etgen A, Fahrbach S, Rabin R (eds) Hormones, brain and behavior, vol 4, 1st edn. Elsevier, AmsterdamGoogle Scholar
  3. Bullock SP, Rogers LJ (1992) Hemispheric specialization for the control of copulation in the young chick and its effects of 5 alpha-dihydrotestosterone and 17 beta-oE2. Behav Brain Res 48:9–14PubMedCrossRefGoogle Scholar
  4. Chura LR, Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Bullmore ET, Baron-Cohen S (2010) Organizational effects of fetal testosterone on human corpus callosum size and asymmetry. Psychoneuroendocrinology 35:122–132PubMedCrossRefGoogle Scholar
  5. Clark MM, vom Saal FS, Galef BG (1992) Intrauterine positions and testosterone levels of adult male gerbils are correlated. Physiol Behav 51:957–960PubMedCrossRefGoogle Scholar
  6. Cohen-Bendahan CC, Buitelaar JK, van Goozen SH, Cohen-Kettenis PT (2004) Prenatal exposure to testosterone and functional cerebral lateralisation: a study in same-sex and opposite-sex twin girls. Psychoneuroendocrinology 29:911–916PubMedCrossRefGoogle Scholar
  7. Decuypere E, Bruggeman V, Onagbesan O, Safi M (2002) Endocrine physiology of reproduction in the female chicken: old wine in new bottles. Avian Poult Biol Rev 13:145–153CrossRefGoogle Scholar
  8. Dharmaretnam M, Vijitha V, Priyadharshihi K, Jashini T, Vathany K (2002) Ground scratching and preferred leg use in domestic chicks: changes in motor control in the first two weeks post-hatching. Laterality 7:371–380PubMedCrossRefGoogle Scholar
  9. Elf PK, Fivizzani AJ (2002) Changes in sex steroid levels in yolks of the leghorn chicken, Gallus domesticus, during embryonic development. J Exp Zool 293:594–600PubMedCrossRefGoogle Scholar
  10. Gallup GGJ (1979) Tonic immobility as a measure of fear in domestic fowl. Anim Behav 27:316–317CrossRefGoogle Scholar
  11. Geschwind N, Behan P (1984) Hormones, handedness and immunity. Immunol Today 5:190–191CrossRefGoogle Scholar
  12. Geschwind N, Galaburda AM (1985) Cerebral lateralization—biological mechanisms, associations, and pathology.1. A hypothesis and a program for research. Arch Neurol 42:428–459PubMedCrossRefGoogle Scholar
  13. Gil D (2008) Hormones in avian eggs: physiology, ecology and behaviour. Adv Stud Behav 38:337–398CrossRefGoogle Scholar
  14. Grimshaw GM, Bryden MP, Finegan JK (1993) Relations between prenatal testosterone and cerebral lateralization at Age 10. J Clin Expl Neuropsych 15:39–40Google Scholar
  15. Grimshaw GM, Bryden MP, Finegan JAK (1995) Relations between prenatal testosterone and cerebral lateralization in children. Neuropsychology 9:68–79CrossRefGoogle Scholar
  16. Groothuis TGG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter, but what do we know of them? Phil Trans Royal Soc B 363:1647–1661CrossRefGoogle Scholar
  17. Groothuis TGG, Muller W, von Engelhardt N, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29:329–352PubMedCrossRefGoogle Scholar
  18. Güntürkün O, Hellmann B, Melsbach G, Prior H (1998) Asymmetries of representation in the visual system of pigeons. NeuroReport 9:4127–4130PubMedCrossRefGoogle Scholar
  19. Halpern ME, Güntürkün O, Hopkins WD, Rogers LJ (2005) Lateralization of the vertebrate brain: taking the side of model systems. J Neurosci 25:10351–10357PubMedCrossRefGoogle Scholar
  20. Hausmann M, Güntürkün O (2000) Steroid fluctuations modify functional cerebral asymmetries: the hypothesis of progesterone-mediated interhemispheric decoupling. Neuropsychologia 38:1362–1374PubMedCrossRefGoogle Scholar
  21. Hausmann M, Slabbekoorn D, van Goozen SHM, Cohen-Kettenis PT, Güntürkün O (2000) Sex hormones affect spatial abilities during the menstrual cycle. Behav Neurosci 114:1245–1250PubMedCrossRefGoogle Scholar
  22. Hirnstein M, Hausmann M, Güntürkün O (2008) The evolutionary origins of functional cerebral asymmetries in humans: does lateralization enhance parallel processing? Behav Brain Res 187:297–303PubMedCrossRefGoogle Scholar
  23. Holman SD, Hutchison JB (1991) Lateralized action of androgen on development of behavior and brain sex differences. Brain Res Bull 27:261–265PubMedCrossRefGoogle Scholar
  24. Jones RB (1986) The tonic immobility reaction of the domestic fowl: a review. World Poultry Sci J 42:82–96CrossRefGoogle Scholar
  25. Lust JM, Geuze RH, van de Beek C, Cohen-Kettenis PT, Groothuis AGG, Bouma A (2010) Sex specific effect of prenatal testosterone on language lateralization in children. Neuropsychologia 48:536–540PubMedCrossRefGoogle Scholar
  26. Lust JM, Geuze RH, Groothuis AGG, Bouma A (2011a) Functional cerebral lateralization and dual-task efficiency-testing the function of human brain lateralization using fTCD. Behav Brain Res 217:293–301PubMedCrossRefGoogle Scholar
  27. Lust JM, Geuze RH, Groothuis AGG, van der Zwan JE, Brouwer WH, van Wolffelaar PC, Bouma A (2011b) Driving performance during word generation—testing the function of human brain lateralization using fTCD in an ecologically relevant context. Neuropsychologia 49:2375–2383PubMedCrossRefGoogle Scholar
  28. Lust JM, Geuze RH, van de Beek C, Cohen-Kettenis PT, Bouma A, Groothuis AGG (2011c) Differential effects of prenatal testosterone on lateralization of handedness and language. Neuropsychology 25:581–589PubMedCrossRefGoogle Scholar
  29. Manns M, Güntürkün O (1999) Monocular deprivation alters the direction of functional and morphological asymmetries in the pigeon’s (Columba livia) visual system. Behav Neurosci 113:1257–1266PubMedCrossRefGoogle Scholar
  30. Mills AD, Crawford LL, Domjan M, Faure JM (1997) The behavior of the Japanese or domestic quail Coturnix japonica. Neurosci Biobehav Rev 21:261–281PubMedCrossRefGoogle Scholar
  31. Nottelmann F, Wohlslager A, Güntürkün O (2002) Unihemispheric memory in pigeons-knowledge, the left hemisphere is reluctant to share. Behav Brain Res 133:309–315PubMedCrossRefGoogle Scholar
  32. Pfannkuche KA, Bouma A, Groothuis TGG (2009) Does testosterone affect lateralization of brain and behaviour? A meta-analysis in humans and other animal species. Philos Trans Royal Soc B 364:929–942Google Scholar
  33. Pfannkuche KA, Gahr M, Weites IM, Riedstra B, Wolf C, Groothuis TGG (2011) Examining a pathway for hormone mediated maternal effects—yolk testosterone affects androgen receptor expression and endogenous testosterone production in young chicks (Gallus gallus domesticus). Gen Comp Endocr 172:487–493PubMedCrossRefGoogle Scholar
  34. Rajendra S, Rogers LJ (1993) Asymmetry is present in the thalamofugal visual projections of female chicks. Exp Brain Res 92:542–544PubMedCrossRefGoogle Scholar
  35. Regolin L, Vallortigara G, Zanforlin M (1995) Detour behaviour in the domestic chick: searching for a disappearing prey or a disappearing social partner. Anim Behav 50:203–211CrossRefGoogle Scholar
  36. Regolin L, Pagni P, Vallortigara G (1998) Brain lateralisation of detour behaviour in the domestic chick (Gallus gallus). Eur J Neurosci 10:15407Google Scholar
  37. Rogers LJ (1982) Light experience and asymmetry of brain function in chickens. Nature 297:223–225PubMedCrossRefGoogle Scholar
  38. Rogers LJ (1990) Light input and the reversal of functional lateralization in the chicken brain. Behav Brain Res 38:211–221PubMedCrossRefGoogle Scholar
  39. Rogers LJ (1995) The development of brain and behaviour in the chicken. CAB International, WallingfordGoogle Scholar
  40. Rogers L (1996) Behavioral, structural and neurochemical asymmetries in the avian brain: a model system for studying visual development and processing. Neurosci Biobehav Rev 20:487–503PubMedCrossRefGoogle Scholar
  41. Rogers LJ (2000) Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang 73:236–253PubMedCrossRefGoogle Scholar
  42. Rogers LJ (2002) Lateralization in vertebrates: its early evolution. General pattern, and development. Adv Study Behav 31:107–161CrossRefGoogle Scholar
  43. Rogers LJ (2006) Factors influencing development of lateralization. Cortex 42:107–109PubMedCrossRefGoogle Scholar
  44. Rogers LJ, Deng C (1999) Light experience and lateralization of the two visual pathways in the chick. Behav Brain Res 98:277–287PubMedCrossRefGoogle Scholar
  45. Rogers LJ, Workman L (1993) Footedness in birds. Anim Behav 45:409–411CrossRefGoogle Scholar
  46. Schwarz IM, Rogers LJ (1992) Testosterone: a role in the development of brain asymmetry in the chick. Neurosci Lett 146:167–170PubMedCrossRefGoogle Scholar
  47. Smith LL, Hines M (2000) Language lateralization and handedness in women prenatally exposed to diethylstilbestrol (DES). Psychoneuroendocrinology 25:497–512PubMedCrossRefGoogle Scholar
  48. Sommer IE, Aleman A, Somers M, Boks MP, Kahn RS (2008) Sex differences in handedness, asymmetry of the Planum Temporale and functional language lateralization. Brain Res 1206:76–88PubMedCrossRefGoogle Scholar
  49. Tommasi L, Vallortigara G (1999) Footedness in binocular and monocular chicks. Laterality 4:89–95PubMedGoogle Scholar
  50. Vallortigara G (1992) Right hemisphere advantage for social recognition in the chick. Neuropsychologia 30:761–768PubMedCrossRefGoogle Scholar
  51. Vallortigara G (2000) Comparative neuropsychology of the dual brain: a stroll through animals’ left and right perceptual worlds. Brain Lang 73:189–219PubMedCrossRefGoogle Scholar
  52. Vallortigara G, Andrew RJ (1991) Lateralization of response by chicks to change in a model partner. Anim Behav 41:187–194CrossRefGoogle Scholar
  53. Vallortigara G, Andrew RJ (1994) Differential involvement of right and left hemisphere in individual recognition in the domestic chick. Behav Process 33:41–58CrossRefGoogle Scholar
  54. Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–589PubMedGoogle Scholar
  55. Vallortigara G, Regolin L, Pagni P (1999a) Detour behaviour, imprinting and visual lateralisation in the domestic chick. Cogn Brain Res 7:307–320CrossRefGoogle Scholar
  56. Vallortigara G, Rogers LJ, Bisazza A (1999b) Possible evolutionary origins of cognitive brain lateralisation. Brain Res Rev 30:164–175PubMedCrossRefGoogle Scholar
  57. von Engelhardt N, Groothuis TGG (2011) Maternal hormones in avian eggs. In: Norris DO, Lopez KH (eds) Hormones and reproduction of vertebrates: Birds, vol 4, 1st edn. Academic Press, San DiegoGoogle Scholar
  58. Voyer D (1996) On the magnitude of laterality effects and sex differences in functional lateralities. Laterality 1:51–84PubMedGoogle Scholar
  59. Weidner C, Reperant J, Miceli D, Haby M, Rio JP (1985) An anatomical study of ipsilateral retinal projections in the quail using autoradiographic, horseradish-peroxidase, fluorescence and degeneration techniques. Brain Res 340:99–108PubMedCrossRefGoogle Scholar
  60. Witelson SF, Nowakowski RS (1991) Left out axons make men right—a hypothesis for the origin of handedness and functional asymmetry. Neuropsychologia 29:327–333PubMedCrossRefGoogle Scholar
  61. Zappia JV, Rogers LJ (1987) Sex differences and reversal of brain asymmetry by testosterone in chickens. Behav Brain Res 23:261–267PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Bernd J. Riedstra
    • 1
  • Kristina A. Pfannkuche
    • 1
  • Antonius G. G. Groothuis
    • 1
  1. 1.Behavioural Biology, Centre for Behaviour and NeurosciencesUniversity of GroningenGroningenThe Netherlands

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