Investigating Effects of Steroid Hormones on Lateralization of Brain and Behavior

  • Tess Beking
  • Reint H. Geuze
  • Ton G. G. Groothuis
Part of the Neuromethods book series (NM, volume 122)


Steroid hormones have been proposed to influence the development of lateralization of brain and behavior. We briefly describe the available hypotheses explaining this influence. These are all based on human data. However, experimental testing is almost exclusively limited to other animal models. As a consequence, different research fields investigate the relationship between steroid hormones and lateralization, all using different techniques and study species. The aim of this chapter is to present an overview of available techniques to study this relationship with an interdisciplinary approach. To this end we describe the basics of hormone secretion and mechanisms of action for androgens, estrogens, progesterone, and corticosteroids. Next, general issues related to hormone sampling and hormone assays are discussed. We then present a critical overview of correlational and experimental methods to study the influence of prenatal and postnatal hormones on lateralization. These methods include hormone measurement in amniotic fluid, saliva, urine, feces, and blood plasma or serum of fetus, mother, and umbilical cord. We also discuss hormone-mediated maternal effects, the manipulation of hormone levels in the embryo or mother, hormone treatment in persons with Gender Dysphoria, and the 2D:4D finger length ratio as a proxy for prenatal testosterone exposure. We argue that lateralization can and should be studied at different levels of organization. Namely, structural and functional brain lateralization, perception and cognition, lateralized motor output and performance. We present tests for these different levels and argue that keeping these levels apart is important, as well as realizing that lateralization and the hormonal influence on it may be different at different levels, for different functions and different species. We conclude that the study of hormonal influences on lateralization of brain and behavior has not yet exploited the knowledge and wide array of techniques currently available, leaving an interesting research field substantially under-explored.

Key words

Animals Human Correlational Experimental Prenatal Postnatal Testosterone Estrogens Hormone sampling Organizing effects 


  1. 1.
    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 R Soc B Biol Sci 364:929–942. doi: 10.1098/rstb.2008.0282 CrossRefGoogle Scholar
  2. 2.
    Cooke B, Hegstrom CD, Villeneuve LS, Breedlove SM (1998) Sexual differentiation of the vertebrate brain: principles and mechanisms. Front Neuroendocrinol 19:323–362. doi: 10.1006/frne.1998.0171 CrossRefPubMedGoogle Scholar
  3. 3.
    Schaafsma SM, Riedstra BJ, Pfannkuche KA et al (2009) Epigenesis of behavioural lateralization in humans and other animals. Philos Trans R Soc Lond B Biol Sci 364:915–927. doi: 10.1098/rstb.2008.0244 CrossRefPubMedGoogle Scholar
  4. 4.
    Hardyck C, Petrinovich LF (1977) Left-handedness. Psychol Bull 84:385–404. doi: 10.1037/0033-2909.84.3.385 CrossRefPubMedGoogle Scholar
  5. 5.
    Jordan HE (1911) The inheritance of left-handedness. Am Breeders Mag 19–29:113–124Google Scholar
  6. 6.
    Annett M (1972) The distribution of manual asymmetry. Br J Psychol 63:343–358. doi: 10.1111/j.2044-8295.1972.tb01282.x CrossRefPubMedGoogle Scholar
  7. 7.
    Annett M (1985) Left, right, hand and brain: the right shift theory. Erlbaum, VAGoogle Scholar
  8. 8.
    Annett M (2002) Handedness and brain asymmetry: the right shift theory. Psychology Press, East SussexGoogle Scholar
  9. 9.
  10. 10.
    McManus IA (1999) Handedness, cerebral lateralization and the evolution of language. In: Corballis MC, Lea SEG (eds) The descent of mind: psychological perspectives on homonid evolution. Oxford University Press, Oxford, pp 194–217Google Scholar
  11. 11.
    Klar AJS (1996) A single locus, RGHT, specifies preference for hand utilization in humans. Cold Spring Harb Symp Quant Biol 61:59–65. doi: 10.1101/SQB.1996.061.01.009 CrossRefPubMedGoogle Scholar
  12. 12.
    Somers M, Ophoff RA, Aukes MF et al (2015) Linkage analysis in a Dutch population isolate shows no major gene for left-handedness or atypical language lateralization. J Neurosci 35:8730–8736. doi: 10.1523/JNEUROSCI.3287-14.2015 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Corballis MC (2014) Left brain, right brain: facts and fantasies. PLoS Biol 12:e1001767. doi: 10.1371/journal.pbio.1001767 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Lien Y-J, Chen WJ, Hsiao P-C, Tsuang H-C (2015) Estimation of heritability for varied indexes of handedness. Laterality 20:469–482. doi: 10.1080/1357650X.2014.1000920 CrossRefPubMedGoogle Scholar
  15. 15.
    Arning L, Ocklenburg S, Schulz S et al (2015) Handedness and the X chromosome: the role of androgen receptor CAG-repeat length. Sci Rep 5:8325. doi: 10.1038/srep08325 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Nelson RJ (2005) An introduction to behavioral endocrinology, 3rd edn. Sinauer Associates, SunderlandGoogle Scholar
  17. 17.
    Adkins-Regan E (2005) Hormones and animal social behavior. Princeton University Press, PrincetonGoogle Scholar
  18. 18.
    Seredynski AL, Balthazart J, Ball GF, Cornil CA (2015) Estrogen receptor β activation rapidly modulates male sexual motivation through the transactivation of metabotropic glutamate receptor 1a. J Neurosci 35:13110–13123. doi: 10.1523/JNEUROSCI.2056-15.2015 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Eberling P, Koivisto VA (1994) Physiological importance of dehydroepiandrosterone. Lancet 343:1479–1481. doi: 10.1016/S0140-6736(94)92587-9 CrossRefGoogle Scholar
  20. 20.
    Nair KS, Rizza RA, O’Brien P et al (2006) DHEA in elderly women and DHEA or testosterone in elderly men. N Engl J Med 355:1647–1659. doi: 10.1056/NEJMoa054629 CrossRefPubMedGoogle Scholar
  21. 21.
    Soma KK (2006) Testosterone and aggression: berthold, birds and beyond. J Neuroendocrinol 18:543–551. doi: 10.1111/j.1365-2826.2006.01440.x CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Weinstock M (2007) Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 32:1730–1740. doi: 10.1007/s11064-007-9339-4 CrossRefPubMedGoogle Scholar
  23. 23.
    Anderson DK, Rhees RW, Fleming DE (1985) Effects of prenatal stress on differentiation of the sexually dimorphic nucleus of the preoptic area (SDN-POA) of the rat brain. Brain Res 332:113–118. doi: 10.1016/0006-8993(85)90394-4 CrossRefPubMedGoogle Scholar
  24. 24.
    Kaiser S, Kruijver FPM, Swaab DF, Sachser N (2003) Early social stress in female guinea pigs induces a masculinization of adult behavior and corresponding changes in brain and neuroendocrine function. Behav Brain Res 144:199–210. doi: 10.1016/S0166-4328(03)00077-9 CrossRefPubMedGoogle Scholar
  25. 25.
    Arnold AP, Breedlove SM (1985) Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm Behav 19:469–498. doi: 10.1016/0018-506X(85)90042-X CrossRefPubMedGoogle Scholar
  26. 26.
    McCarthy MM, Arnold AP (2011) Reframing sexual differentiation of the brain. Nat Neurosci 14:677–683. doi: 10.1038/nn.2834 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Romeo RD (2003) Puberty: a period of both organizational and activational effects of steroid hormones on neurobehavioural development. J Neuroendocrinol 15:1185–1192. doi: 10.1111/j.1365-2826.2003.01106.x CrossRefPubMedGoogle Scholar
  28. 28.
    Hines M, Shipley C (1984) Prenatal exposure to diethylstilbestrol (DES) and the development of sexually dimorphic cognitive abilities and cerebral lateralization. Dev Psychol 20:81–94. doi: 10.1037/0012-1649.20.1.81 CrossRefGoogle Scholar
  29. 29.
    Geschwind N, Galaburda AM (1985) Cerebral lateralization: biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Arch Neurol 42:428. doi: 10.1001/archneur.1985.04060050026008 CrossRefPubMedGoogle Scholar
  30. 30.
    Witelson SF, Nowakowski RS (1991) Left out axons make men right: a hypothesis for the origin of handedness and functional asymmetry. Neuropsychologia 29:327–333CrossRefPubMedGoogle Scholar
  31. 31.
    Henriksen R, Rettenbacher S, Groothuis TGG (2013) Maternal corticosterone elevation during egg formation in chickens (Gallus gallus domesticus) influences offspring traits, partly via prenatal undernutrition. Gen Comp Endocrinol 191:83–91. doi: 10.1016/j.ygcen.2013.05.028 CrossRefPubMedGoogle Scholar
  32. 32.
    Freire R, van Dort S, Rogers LJ (2006) Pre- and post-hatching effects of corticosterone treatment on behavior of the domestic chick. Horm Behav 49:157–165. doi: 10.1016/j.yhbeh.2005.05.015 CrossRefPubMedGoogle Scholar
  33. 33.
    Shirtcliff EA, Granger DA, Schwartz E, Curran MJ (2001) Use of salivary biomarkers in biobehavioral research: cotton-based sample collection methods can interfere with salivary immunoassay results. Psychoneuroendocrinology 26:165–173CrossRefPubMedGoogle Scholar
  34. 34.
    Goymann W (2005) Noninvasive monitoring of hormones in bird droppings: physiological validation, sampling, extraction, sex differences, and the influence of diet on hormone metabolite levels. Ann N Y Acad Sci 1046:35–53. doi: 10.1196/annals.1343.005 CrossRefPubMedGoogle Scholar
  35. 35.
    Gow R, Thomson S, Rieder M et al (2010) An assessment of cortisol analysis in hair and its clinical applications. Forensic Sci Int 196:32–37. doi: 10.1016/j.forsciint.2009.12.040 CrossRefPubMedGoogle Scholar
  36. 36.
    Cook NJ (2012) Review: Minimally invasive sampling media and the measurement of corticosteroids as biomarkers of stress in animals. Can J Anim Sci 92:227–259. doi: 10.4141/cjas2012-045 CrossRefGoogle Scholar
  37. 37.
    von Engelhardt N, Groothuis TGG (2005) Measuring steroid hormones in avian eggs. Ann N Y Acad Sci 1046:181–192. doi: 10.1196/annals.1343.015 CrossRefGoogle Scholar
  38. 38.
    Pfannkuche KA, Gahr M, Weites IM et al (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 Endocrinol 172:487–493. doi: 10.1016/j.ygcen.2011.04.014 CrossRefPubMedGoogle Scholar
  39. 39.
    vom Saal FS (1990) Paradoxical effects of maternal stress on fetal steroids and postnatal reproductive traits in female mice from different intrauterine positions. Biol Reprod 43:751–761. doi: 10.1095/biolreprod43.5.751 CrossRefPubMedGoogle Scholar
  40. 40.
    Winter JSD, Faiman C, Reyes FI (1977) Morphogenesis and malformations of the genital system. A. Liss, New YorkGoogle Scholar
  41. 41.
    Wilson CA, Davies DC (2007) The control of sexual differentiation of the reproductive system and brain. Reproduction 133:331–359. doi: 10.1530/REP-06-0078 CrossRefPubMedGoogle Scholar
  42. 42.
    Knickmeyer RC, Baron-Cohen S (2006) Fetal testosterone and sex differences. Early Hum Dev 82:755–760. doi: 10.1016/j.earlhumdev.2006.09.014 CrossRefGoogle Scholar
  43. 43.
    Judd HL, Robinson JD, Young PE, Jones OW (1976) Amniotic fluid testosterone levels in midpregnancy. Obstet Gynecol 48:690–692PubMedGoogle Scholar
  44. 44.
    Schindler AE (1982) Hormones in human amniotic fluid. Springer, HeidelbergCrossRefGoogle Scholar
  45. 45.
    van de Beek C, Thijssen JHH, Cohen-Kettenis PT et al (2004) Relationships between sex hormones assessed in amniotic fluid, and maternal and umbilical cord serum: what is the best source of information to investigate the effects of fetal hormonal exposure? Horm Behav 46:663–669. doi: 10.1016/j.yhbeh.2004.06.010 CrossRefPubMedGoogle Scholar
  46. 46.
    Finegan JA, Bartleman B, Wong PY (1989) A window for the study of prenatal sex hormone influences on postnatal development. J Genet Psychol 150:101–112. doi: 10.1080/00221325.1989.9914580 CrossRefPubMedGoogle Scholar
  47. 47.
    Robinson JD, Judd HL, Young PE et al (1977) Amniotic fluid androgens and estrogens in midgestation. J Clin Endocrinol Metab 45:755–761. doi: 10.1210/jcem-45-4-755 CrossRefPubMedGoogle Scholar
  48. 48.
    Sikich L, Todd RD (1988) Are the neurodevelopmental effects of gonadal hormones related to sex differences in psychiatric illnesses? Psychiatr Dev 6:277–309PubMedGoogle Scholar
  49. 49.
    Groothuis TGG, von Engelhardt N (2005) Investigating maternal hormones in avian eggs: measurement, manipulation, and interpretation. Ann N Y Acad Sci 1046:168–180. doi: 10.1196/annals.1343.014 CrossRefPubMedGoogle Scholar
  50. 50.
    Schaafsma SM, Groothuis TGG (2012) Sex-specific effects of maternal testosterone on lateralization in a cichlid fish. Anim Behav 83:437–443. doi: 10.1016/j.anbehav.2011.11.015 CrossRefGoogle Scholar
  51. 51.
    Ford JJ (1980) Serum testosterone concentrations in embryonic and fetal pigs during sexual differentiation. Biol Reprod 23:583–587. doi: 10.1095/biolreprod23.3.583 CrossRefPubMedGoogle Scholar
  52. 52.
    Hönekopp J, Bartholdt L, Beier L, Liebert A (2007) Second to fourth digit length ratio (2D:4D) and adult sex hormone levels: new data and a meta-analytic review. Psychoneuroendocrinology 32:313–321CrossRefPubMedGoogle Scholar
  53. 53.
    Putz DA, Gaulin SJC, Sporter RJ, McBurney DH (2004) Sex hormones and finger length. what does 2D:4D indicate? Evol Hum Behav 25:182–199. doi: 10.1016/j.evolhumbehav.2004.03.005 CrossRefGoogle Scholar
  54. 54.
    Lutchmaya S, Baron-Cohen S, Raggatt P et al (2004) 2nd to 4th digit ratios, fetal testosterone and estradiol. Early Hum Dev 77:23–28. doi: 10.1016/j.earlhumdev.2003.12.002 CrossRefPubMedGoogle Scholar
  55. 55.
    Ventura T, Gomes MC, Pita A et al (2013) Digit ratio (2D:4D) in newborns: influences of prenatal testosterone and maternal environment. Early Hum Dev 89:107–112. doi: 10.1016/j.earlhumdev.2012.08.009 CrossRefPubMedGoogle Scholar
  56. 56.
    McFadden D, Bracht MS (2005) Sex differences in the relative lengths of metacarpals and metatarsals in gorillas and chimpanzees. Horm Behav 47:99–111. doi: 10.1016/j.yhbeh.2004.08.013 CrossRefPubMedGoogle Scholar
  57. 57.
    Auger J, Le Denmat D, Berges R et al (2013) Environmental levels of oestrogenic and antiandrogenic compounds feminize digit ratios in male rats and their unexposed male progeny. Proc Biol Sci 280:20131532. doi: 10.1098/rspb.2013.1532 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Dean A, Sharpe RM (2013) Clinical review: Anogenital distance or digit length ratio as measures of fetal androgen exposure: relationship to male reproductive development and its disorders. J Clin Endocrinol Metab 98:2230–2238. doi: 10.1210/jc.2012-4057 CrossRefPubMedGoogle Scholar
  59. 59.
    Nagy G, Blázi G, Hegyi G, Török J (2016) Side-specific effect of yolk testosterone elevation on second-to-fourth digit ratio in a wild passerine. Naturwissenschaften 103:4. doi: 10.1007/s00114-015-1328-x CrossRefPubMedGoogle Scholar
  60. 60.
    Ruuskanen S, Helle S, Ahola M et al (2011) Digit ratios have poor indicator value in a wild bird population. Behav Ecol Sociobiol 65:983–994. doi: 10.1007/s00265-010-1099-5 CrossRefPubMedGoogle Scholar
  61. 61.
    Romano M, Rubolini D, Martinelli R et al (2005) Experimental manipulation of yolk testosterone affects digit length ratios in the ring-necked pheasant (Phasianus colchicus). Horm Behav 48:342–346. doi: 10.1016/j.yhbeh.2005.03.007 CrossRefPubMedGoogle Scholar
  62. 62.
    Zielinski WJ, vom Saal FS, Vandenbergh JG (1992) The effect of intrauterine position on the survival, reproduction and home range size of female house mice (Mus musculus). Behav Ecol Sociobiol 30:185–191. doi: 10.1007/BF00166702 CrossRefGoogle Scholar
  63. 63.
    Clark M, Galef B (1998) Effects of intrauterine position on the behavior and genital morphology of litter-bearing rodents. Dev Neuropsychol 14:197–211CrossRefGoogle Scholar
  64. 64.
    Tapp AL, Maybery MT, Whitehouse AJO (2011) Evaluating the twin testosterone transfer hypothesis: a review of the empirical evidence. Horm Behav 60:713–722. doi: 10.1016/j.yhbeh.2011.08.011 CrossRefPubMedGoogle Scholar
  65. 65.
    Okuliarova M, Groothuis TGG, Skrobánek P, Zeman M (2011) Experimental evidence for genetic heritability of maternal hormone transfer to offspring. Am Nat 177:824–834. doi: 10.1086/659996 CrossRefPubMedGoogle Scholar
  66. 66.
    Costantini D, Metcalfe NB, Monaghan P (2010) Ecological processes in a hormetic framework. Ecol Lett 13:1435–1447. doi: 10.1111/j.1461-0248.2010.01531.x CrossRefPubMedGoogle Scholar
  67. 67.
    Del Giudice M (2012) Fetal programming by maternal stress: insights from a conflict perspective. Psychoneuroendocrinology 37:1614–1629. doi: 10.1016/j.psyneuen.2012.05.014 CrossRefPubMedGoogle Scholar
  68. 68.
    von Engelhardt N, Groothuis TGG (2011) Hormones and reproduction of vertebrates. doi: 10.1016/B978-0-12-374929-1.10004-6
  69. 69.
    Henriksen R, Rettenbacher S, Groothuis TGG (2011) Prenatal stress in birds: pathways, effects, function and perspectives. Neurosci Biobehav Rev 35:1484–1501. doi: 10.1016/j.neubiorev.2011.04.010 CrossRefPubMedGoogle Scholar
  70. 70.
    Rogers LJ, Deng C (2005) Corticosterone treatment of the chick embryo affects light-stimulated development of the thalamofugal visual pathway. Behav Brain Res 159:63–71. doi: 10.1016/j.bbr.2004.10.003 CrossRefPubMedGoogle Scholar
  71. 71.
    Schwarz IM, Rogers LJ (1992) Testosterone: a role in the development of brain asymmetry in the chick. Neurosci Lett 146:167–170. doi: 10.1016/0304-3940(92)90069-J CrossRefPubMedGoogle Scholar
  72. 72.
    Groothuis TGG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philos Trans R Soc Lond B Biol Sci 363:1647–1661. doi: 10.1098/rstb.2007.0007 CrossRefPubMedGoogle Scholar
  73. 73.
    Hines M (2006) Prenatal testosterone and gender-related behaviour. Eur J Endocrinol 155(Suppl):S115–S121. doi: 10.1530/eje.1.02236 CrossRefPubMedGoogle Scholar
  74. 74.
    Hodgetts S, Weis S, Hausmann M (2015) Sex hormones affect language lateralisation but not cognitive control in normally cycling women. Horm Behav 74:194–200. doi: 10.1016/j.yhbeh.2015.06.019 CrossRefPubMedGoogle Scholar
  75. 75.
    Fischer H, Sandblom J, Gavazzeni J et al (2005) Age-differential patterns of brain activation during perception of angry faces. Neurosci Lett 386:99–104. doi: 10.1016/j.neulet.2005.06.002 CrossRefPubMedGoogle Scholar
  76. 76.
    Wright ND, Bahrami B, Johnson E et al (2012) Testosterone disrupts human collaboration by increasing egocentric choices. Proc Biol Sci 279:2275–2280. doi: 10.1098/rspb.2011.2523 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Kreukels BPC, Cohen-Kettenis PT (2011) Puberty suppression in gender identity disorder: the Amsterdam experience. Nat Rev Endocrinol 7:466–472. doi: 10.1038/nrendo.2011.78 CrossRefPubMedGoogle Scholar
  78. 78.
    Hembree WC, Cohen-Kettenis P, Delemarre-van de Waal HA et al (2009) Endocrine treatment of transsexual persons: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 94:3132–3154. doi: 10.1210/jc.2009-0345 CrossRefPubMedGoogle Scholar
  79. 79.
    Marshall WA, Tanner JM (1969) Variations in pattern of pubertal changes in girls. Arch Dis Child 44:291–303CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Marshall WA, Tanner JM (1970) Variations in the pattern of pubertal changes in boys. Arch Dis Child 45:13–23CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Brenowitz EA (2004) Plasticity of the adult avian song control system. Ann N Y Acad Sci 1016:560–585. doi: 10.1196/annals.1298.006 CrossRefPubMedGoogle Scholar
  82. 82.
    Moorman S, Gobes SMH, Kuijpers M et al (2012) Human-like brain hemispheric dominance in birdsong learning. Proc Natl Acad Sci U S A 109:12782–12787. doi: 10.1073/pnas.1207207109 CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Neveu PJ, Liège S, Sarrieau A (1998) Asymmetrical distribution of hippocampal mineralocorticoid receptors depends on lateralization in mice. Neuroimmunomodulation 5:16–21CrossRefPubMedGoogle Scholar
  84. 84.
    Gahr M (2007) Sexual differentiation of the vocal control system of birds. Adv Genet 59:67–105. doi: 10.1016/S0065-2660(07)59003-6 PubMedGoogle Scholar
  85. 85.
    Adret P, Rogers LJ (1989) Sex difference in the visual projections of young chicks: a quantitative study of the thalamofugal pathway. Brain Res 478:59–73. doi: 10.1016/0006-8993(89)91477-7 CrossRefPubMedGoogle Scholar
  86. 86.
    Fink M, Wadsak W, Savli M et al (2009) Lateralization of the serotonin-1A receptor distribution in language areas revealed by PET. Neuroimage 45:598–605. doi: 10.1016/j.neuroimage.2008.11.033 CrossRefPubMedGoogle Scholar
  87. 87.
    Vernaleken I, Weibrich C, Siessmeier T et al (2007) Asymmetry in dopamine D(2/3) receptors of caudate nucleus is lost with age. Neuroimage 34:870–878. doi: 10.1016/j.neuroimage.2006.10.013 CrossRefPubMedGoogle Scholar
  88. 88.
    Wang H, Wang X, Wetzel W, Scheich H (2006) Rapid-rate transcranial magnetic stimulation of animal auditory cortex impairs short-term but not long-term memory formation. Eur J Neurosci 23:2176–2184. doi: 10.1111/j.1460-9568.2006.04745.x CrossRefPubMedGoogle Scholar
  89. 89.
    Rotenberg A, Muller PA, Vahabzadeh-Hagh AM et al (2010) Lateralization of forelimb motor evoked potentials by transcranial magnetic stimulation in rats. Clin Neurophysiol 121:104–108. doi: 10.1016/j.clinph.2009.09.008 CrossRefPubMedGoogle Scholar
  90. 90.
    Willis MW, Ketter TA, Kimbrell TA et al (2002) Age, sex and laterality effects on cerebral glucose metabolism in healthy adults. Psychiatry Res 114:23–37CrossRefPubMedGoogle Scholar
  91. 91.
    Stroobant N, Vingerhoets G (2000) Transcranial Doppler ultrasonography monitoring of cerebral hemodynamics during performance of cognitive tasks: a review. Neuropsychol Rev 10:213–231CrossRefPubMedGoogle Scholar
  92. 92.
    Deppe M, Ringelstein EB, Knecht S (2004) The investigation of functional brain lateralization by transcranial Doppler sonography. Neuroimage 21:1124–1146. doi: 10.1016/j.neuroimage.2003.10.016 CrossRefPubMedGoogle Scholar
  93. 93.
    Honing H, Merchant H, Háden GP et al (2012) Rhesus monkeys (Macaca mulatta) detect rhythmic groups in music, but not the beat. PLoS One 7:e51369. doi: 10.1371/journal.pone.0051369 CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Rowan A, Liégeois F, Vargha-Khadem F et al (2004) Cortical lateralization during verb generation: a combined ERP and fMRI study. Neuroimage 22:665–675. doi: 10.1016/j.neuroimage.2004.01.034 CrossRefPubMedGoogle Scholar
  95. 95.
    Rogers LJ, Vallortigara G, Andrew RJ (2015) Divided brains: the biology and behaviour of brain asymmetries. Cambridge University Press, CambridgeGoogle Scholar
  96. 96.
    Cashmore L, Uomini N, Chapelain A (2008) The evolution of handedness in humans and great apes: a review and current issues. J Anthropol Sci 86:7–35PubMedGoogle Scholar
  97. 97.
    Lust JM, Geuze RH, Groothuis AGG, Bouma A (2011) Functional cerebral lateralization and dual-task efficiency-testing the function of human brain lateralization using fTCD. Behav Brain Res 217:293–301. doi: 10.1016/j.bbr.2010.10.029 CrossRefPubMedGoogle Scholar
  98. 98.
    Lust JM, Geuze RH, Groothuis AGG et al (2011) Driving performance during word generation—testing the function of human brain lateralization using fTCD in an ecologically relevant context. Neuropsychologia 49:2375–2383. doi: 10.1016/j.neuropsychologia.2011.04.011 CrossRefPubMedGoogle Scholar
  99. 99.
    Hirnstein M, Leask S, Rose J, Hausmann M (2010) Disentangling the relationship between hemispheric asymmetry and cognitive performance. Brain Cogn 73:119–127. doi: 10.1016/j.bandc.2010.04.002 CrossRefPubMedGoogle Scholar
  100. 100.
    Stroobant N, van Boxstael J, Vingerhoets G (2011) Language lateralization in children: a functional transcranial Doppler reliability study. J Neurolinguistics 24:14–24. doi: 10.1016/j.jneuroling.2010.07.003 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media LLC 2017

Authors and Affiliations

  • Tess Beking
    • 1
    • 2
  • Reint H. Geuze
    • 1
  • Ton G. G. Groothuis
    • 2
  1. 1. Clinical & Developmental NeuropsychologyUniversity of GroningenGroningenThe Netherlands
  2. 2.Behavioural Biology, Groningen Institute for Evolutionary Life SciencesUniversity of GroningenGroningenThe Netherlands

Personalised recommendations