How brain asymmetry relates to performance - a large-scale dichotic listening study

Marco Hirnstein, Kenneth Hugdahl, Markus Hausmann, Marco Hirnstein, Kenneth Hugdahl, Markus Hausmann

Abstract

All major mental functions including language, spatial and emotional processing are lateralized but how strongly and to which hemisphere is subject to inter- and intraindividual variation. Relatively little, however, is known about how the degree and direction of lateralization affect how well the functions are carried out, i.e., how lateralization and task performance are related. The present study therefore examined the relationship between lateralization and performance in a dichotic listening task for which we had data available from 1839 participants. In this task, consonant-vowel syllables are presented simultaneously to the left and right ear, such that each ear receives a different syllable. When asked which of the two they heard best, participants typically report more syllables from the right ear, which is a marker of left-hemispheric speech dominance. We calculated the degree of lateralization (based on the difference between correct left and right ear reports) and correlated it with overall response accuracy (left plus right ear reports). In addition, we used reference models to control for statistical interdependency between left and right ear reports. The results revealed a u-shaped relationship between degree of lateralization and overall accuracy: the stronger the left or right ear advantage, the better the overall accuracy. This u-shaped asymmetry-performance relationship consistently emerged in males, females, right-/non-right-handers, and different age groups. Taken together, the present study demonstrates that performance on lateralized language functions depends on how strongly these functions are lateralized. The present study further stresses the importance of controlling for statistical interdependency when examining asymmetry-performance relationships in general.

Keywords: age; dichotic listening; handedness; hemispheric asymmetry; lateralization; sex; task-performance; verbal abilities.

Figures

FIGURE 1
FIGURE 1
Results and principle of the LOESS method. (A) The raw left and right ear reports are used to compute the laterality coefficient and the overall accuracy. Laterality coefficient and overall accuracy are fitted with LOESS (red line). (B) Reference models (blue lines) are computed which are based on the raw left and right ear reports but not correlated (r < 0.01). The reference models are also fitted with LOESS. (C) The reference models are subtracted (C) from the raw data and then averaged (D) to reveal the asymmetry-performance relationship controlled for interdependency.
FIGURE 2
FIGURE 2
Mean left and right ear reports (±SEM) across sex and age. Both males and females in all age groups report more syllables from the right than the left ear. This right ear advantage is slightly stronger in males than females in all age groups except in early adolescents.
FIGURE 3
FIGURE 3
Results of the traditional approach. The bubble chart shows the linear (red line) and quadratic regression (blue line) between overall accuracy and degree of lateralization.
FIGURE 4
FIGURE 4
The relationship between (relative) performance and degree of lateralization with the alternative approach in males (A), females (B), right-handers (C), non-right-handers (D), children aged 5–9 (E), early adolescents aged 10–15 (F), younger adults aged 16–49 (G), and older adults aged 50+ (H).

References

    1. Barth J. M., Boles D. B., Giattina A. A., Penn C. E. (2012). Preschool child and adult lateralisation and performance in emotion and language tasks. Laterality 17 412–427 10.1080/1357650X.2011.626435
    1. Bayer U., Hausmann M. (2009). Estrogen therapy affects right hemisphere functioning in postmenopausal women. Horm. Behav. 55 228–234 10.1016/j.yhbeh.2008
    1. Boles D. B., Barth J. M. (2011). “Does degree of asymmetry relate to performance?” A critical review. Brain Cogn. 76 1–410.1016/j.bandc.2011.01.013
    1. Boles D. B., Barth J. M., Merrill E. C. (2008). Asymmetry and performance: toward a neurodevelopmental theory. Brain Cogn. 66 124–13910.1016/j.bandc.2007.06.002
    1. Broca P. P. (1861). Perte de la parole, ramollissement chronique et destruction partielle du lobe antérieur gauche du cerveau. Bull. Soc. Anthropol. 2 235–238
    1. Bryden M. P. (1988). “An overview of the dichotic listening procedure and its relation to cerebral organization,” in Handbook of Dichotic Listening: Theory, Methods, and Research ed. Hugdahl K. (Chichester, UK: Wiley; ) 1–44
    1. Catani M., Allin M. P. G., Husain M., Pugliese L., Mesulam M. M., Murray R. M., et al. (2007). Symmetries in human brain language pathways correlate with verbal recall. Proc. Natl. Acad. Sci. U.S.A 104 17163–1716810.1073/pnas.0702116104
    1. Chiarello C., Halderman L., Welcome S. E., Leonard C. M. (2011). Does degree of asymmetry relate to performance? A reply to Boles and Barth. Brain Cogn. 77 135–13710.1016/j.bandc.2011.05.005
    1. Chiarello C., Welcome S. E., Halderman L. K., Leonard C. M. (2009). Does degree of asymmetry relate to performance? An investigation of word recognition and reading in consistent and mixed handers. Brain Cogn. 69 521–53010.1016/j.bandc.2008.11.002
    1. Cohen J. (1988). Statistical Power Analysis for the Behavioral Sciences. Hillsdale, NJ: Lawrence Erlbaum Associates
    1. Corballis M. C. (1991). The Lopsided Ape. New York: Oxford University Press
    1. Corballis M. C. (2005). The trade-off between symmetry and asymmetry. Behav. Brain Sci. 28 594–59510.1017/S0140525X05270103
    1. Corballis M. C. (2006). Cerebral asymmetry: a question of balance. Cortex 42 117–11810.1016/S0010-9452(08)70335-6
    1. Corballis M. C. (2009). The evolution and genetics of cerebral asymmetry. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364 867–87910.1098/rstb.2008.0232
    1. Crow T. J. (2002). The Speciation of Modern Homo Sapiens. Oxford, UK: Oxford University Press
    1. Crow T. J., Crow L. R., Done D. J., Leask S. (1998). Relative hand skill predicts academic ability: global deficits at the point of hemispheric indecision. Neuropsychologia 36 1275–128210.1016/S0028-3932(98)00039-6
    1. Davidson R. J., Hugdahl K. (1995). Brain Asymmetry. Cambridge, MA: MIT Press
    1. Dax M. (1865). Lésions de la moitié gauche de l’encéphale coincidant avec l’oubli des signes de la pensée. Gaz Hebd. Med. Chir. (Paris) 33 259–262
    1. Everts R., Lidzba K., Wilke M., Kiefer C., Mordasini M., Schroth G., et al. (2009). Strengthening of laterality of verbal and visuospatial functions during childhood and adolescence. Hum. Brain Mapp. 30 473–48310.1002/hbm.20523
    1. Güntürkün O., Diekamp B., Manns M., Nottelmann F., Prior H., Schwarz A., et al. (2000). Asymmetry pays: visual lateralization improves discrimination success in pigeons. Curr. Biol. 10 1079–108110.1016/S0960-9822(00)00671-0
    1. Hausmann M, Güntürkün O. (2000). Steroid fluctuations modify functional cerebral asymmetries: the hypothesis of progesterone-mediated interhemispheric decoupling. Neuropsychologia 38 1362–137410.1016/S0028-3932(00)00045-2
    1. Hellige J. B. (1993). Hemispheric Asymmetry: What’s Right and What’s Left. Cambridge, MA: Harvard University Press
    1. Hirnstein M. (2011). Dichotic listening and left–right confusion. Brain Cogn. 76 239–24410.1016/j.bandc.2011.02.005
    1. Hirnstein M., Hausmann M, Güntürkün O. (2008). The evolutionary origins of functional cerebral asymmetries in humans: does lateralization enhance parallel processing? Behav. Brain Res. 187 297–30310.1016/j.bbr.2007.09.023
    1. Hirnstein M., Leask S., Rose J., Hausmann M. (2010). Disentangling the relationship between hemispheric asymmetry and cognitive performance. Brain Cogn. 73 119–12710.1016/j.bandc.2010.04.002
    1. Hirnstein M., Westerhausen R., Korsnes M. S., Hugdahl K. (2013). Sex differences in language asymmetry are age-dependent and small: a large-scale, consonant-vowel dichotic listening study with behavioral and fMRI data. Cortex 49 1910–192110.1016/j.cortex.2012.08.002
    1. Hjelmervik H., Westerhausen R., Osnes B., Endresen C. B., Hugdahl K., Hausmann M., et al. (2012). Language lateralization and cognitive control across the menstrual cycle assessed with a dichotic-listening paradigm. Psychoneuroendocrinology 37 1866–187510.1016/j.psyneuen.2012.03.021
    1. Hugdahl K. (2003). “Dichotic listening in the study of auditory laterality,” in The Asymmetrical Brain eds Hugdahl K., Davidson R. J. (Cambridge, MA: MIT Press; ) 441–478
    1. Hugdahl K. (2011). Fifty years of dichotic listening research – still going and going and. Brain Cogn. 76 211–21310.1016/j.bandc.2011.03.006
    1. Hugdahl K., Bronnick K., Kyllingsbaek S., Law I., Gade A., Paulson O. B. (1999). Brain activation during dichotic presentations of consonant-vowel and musical instrument stimuli: a O-15-PET study. Neuropsychologia 37 431–44010.1016/S0028-3932(98)00101-8
    1. Hugdahl K., Carlsson G., Uvebrant P., Lundervold A. J. (1997). Dichotic-listening performance and intracarotid injections of amobarbital in children and adolescents – Preoperative and postoperative comparisons. Arch. Neurol. 54 1494–150010.1001/archneur.1997.00550240046011
    1. Johnston D. W., Nicholls M. E., Shah M., Shields M. A. (2009). Nature’s experiment? Handedness and early childhood development. Demography 46 281–30110.1353/dem.0.0053
    1. Kimura D. (2011). From ear to brain. Brain Cogn. 76 214–21710.1016/j.bandc.2010.11.009
    1. Knecht S., Deppe M., Drager B., Bobe L., Lohmann H., Ringelstein E. B., et al. (2000). Language lateralization in healthy right-handers. Brain 123 74–8110.1093/brain/123.1.74
    1. Ladavas E., Umilta C. (1983). Do laterality measures relate to speed of response in central vision? Brain Cogn. 2 119–12810.1016/0278-2626(83)90002-7
    1. Leask S. J., Crow T. J. (1997). How far does the brain lateralize?: an unbiased method for determining the optimum degree of hemispheric specialization. Neuropsychologia 35 1381–138710.1016/S0028-3932(97)00059-6
    1. Leask S. J., Crow T. J. (2006). A single optimum degree of hemispheric specialisation in two tasks, in two UK national birth cohorts. Brain Cogn. 62 221–22710.1016/j.bandc.2006.06.001
    1. McManus C. (2002). Right Hand, Left Hand: The Origins of Asymmetry in Brains, Bodies, Atoms, and Cultures. London: Weidenfeld & Nicolson
    1. Mellet E., Jobard G., Zago L., Crivello F., Petit L., Joliot M., et al. (2013). Relationships between hand laterality and verbal and spatial skills in 436 healthy adults balanced for handedness. Laterality 10.1080/1357650X.2013.796965 [Epub ahead of print].
    1. Nicholls M. E., Chapman H. L., Loetscher T., Grimshaw G. M. (2010). The relationship between hand preference, hand performance, and general cognitive ability. J. Int. Neuropsychol. Soc. 16 585–592 10.1017/S1355617710000184
    1. Oldfield R. C. (1971). Assessment and analysis of handedness – edinburgh inventory. Neuropsychologia 9 97–11310.1016/0028-3932(71)90067-4
    1. Papousek I., Murhammer D., Schulter G. (2011). Intra- and interindividual differences in lateralized cognitive performance and asymmetrical EEG activity in the frontal cortex. Brain Cogn. 75 225–231 10.1016/j.bandc.2010.11.013
    1. Papousek I., Reiser E. M., Weber B., Freudenthaler H. H., Schulter G. (2012). Frontal brain asymmetry and affective flexibility in an emotional contagion paradigm. Psychophysiology 49 489–49810.1111/j.1469-8986.2011.01324.x
    1. Raczkowski D., Kalat J. W., Nebes R. (1974). Reliability and validity of some handedness questionnaire items. Neuropsychologia 12 43–4710.1016/0028-3932(74)90025-6
    1. Rasmussen T., Milner B. (1977). The role of early left-brain injury in determining lateralization of cerebral speech functions. Ann. N. Y. Acad. Sci. 299 355–36910.1111/j.1749-6632.1977.tb41921.x
    1. Razafimandimby A., Tzourio-Mazoyer N., Mazoyer B., Maiza O., Dollfus S. (2011). Language lateralization in left-handed patients with schizophrenia. Neuropsychologia 49 313–31910.1016/j.neuropsychologia.2010.11.025
    1. Repp B. H. (1977). Measuring laterality effects in dichotic-listening. J. Acoust. Soc. Am. 62 720–73710.1121/1.381584
    1. Rogers L. J., Zucca P., Vallortigara G. (2004). Advantages of having a lateralized brain. Proc. R. Soc. Lond. B Biol. Sci. 271 S420–S42210.1098/rsbl.2004.0200
    1. Vallortigara G., Rogers L. J. (2005). Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav. Brain Sci. 28 575–58910.1017/S0140525X05000105
    1. van Ettinger-Veenstra H. M., Ragnehed M., Hallgren M., Karlsson T., Landtblom A. M., Lundberg P., et al. (2010). Right-hemispheric brain activation correlates to language performance. Neuroimage 49 3481–348810.1016/j.neuroimage.2009.10.041
    1. Wechsler D. (2008). Wechsler Adult Intelligence Scale-Fourth Edition. San Antonio, TX: Pearson

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe