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Cognitive-perceptual load modulates hand selection in left-handers to a greater extent than in right-handers

  • Jiali Liang
  • Krista M. Wilkinson
  • Robert L. Sainburg
Research Article

Abstract

Previous studies have proposed that selecting which hand to use for a reaching task appears to be modulated by a factor described as “task difficulty,” defined by either the requirement for spatial precision or movement sequences. However, we previously reported that analysis of the movement costs associated with even simple movements plays a major role in hand selection. We further demonstrated, in right-handers, that cognitive-perceptual loading modulates hand selection by interfering with the analysis of such costs. It has been reported that left-handers tend to show less dominant hand bias in selecting which hand to use during reaching. We, therefore, hypothesized that hand selection would be less affected by cognitive-perceptual loading in left-handers than in right-handers. We employed a visual search task that presented different levels of difficulty (cognitive-perceptual load), as established in previous studies. Our findings indicate that left-handed participants tend to show greater modulation of hand selection by cognitive-perceptual loading than right-handers. Left-handers showed lower dominant hand reaction times than right-handers, and greater high-cost movements that reached to extremes of the contralateral workspace under the most difficult task conditions. We previously showed in this task that midline crossing has high-energy and time costs and that they occur more frequently under cognitively demanding conditions. The current study revealed that midline crossing was associated with the lowest reaction times, in both handedness groups. The fact that left-handers showed lower dominant hand reaction times, and a greater number of high-cost cross-midline reaches under the most cognitively demanding conditions suggests that these actions were erroneous.

Keywords

Cognitive-perceptual load Hand selection Reaching Task difficulty Left-hander 

Notes

Acknowledgements

This work was supported by the National Institutes of Health [R01HD059783], and a Penn State SSRI Level 1 Award. The second author is co-funded by the Penn State SSRI. The authors thank Christine Regiec, Emily Neumann, and Tara O’Neill for their assistance throughout the development of this research.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

References

  1. Barthélémy S, Boulinguez P (2001) Manual reaction time asymmetries in human subjects: the role of movement planning and attention. Neurosci Lett 315(1):41–44.  https://doi.org/10.1016/S0304-3940(01)02313-8 CrossRefPubMedGoogle Scholar
  2. Barthélémy S, Boulinguez P (2002) Manual asymmetries in the directional coding of reaching: further evidence for hemispatial effects and right hemisphere dominance for movement planning. Exp Brain Res 147(3):305–312.  https://doi.org/10.1007/s00221-002-1247-x CrossRefPubMedGoogle Scholar
  3. Bishop DVM, Ross VA, Daniels MS, Bright P (1996) The measurement of hand preference: a validation study comparing three groups of right-handers. Brit J Psychol (London England: 1953) 87(Pt 2):269–285CrossRefGoogle Scholar
  4. Borod JC, Caron HS, Koff E (1984) Left-handers and right-handers compared on performance and preference measures of lateral dominance. Brit J Psychol 75(2):177–186.  https://doi.org/10.1111/j.2044-8295.1984.tb01889.x CrossRefPubMedGoogle Scholar
  5. Bryden MP (1977) Measuring handedness with questionnaires. Neuropsychologia 15(4–5):617–624CrossRefGoogle Scholar
  6. Bryden PJ, Roy EA (2006) Preferential reaching across regions of hemispace in adults and children. Dev Psychobiol 48(2):121–132.  https://doi.org/10.1002/dev.20120 CrossRefPubMedGoogle Scholar
  7. Bryden PJ, Pryde M, Roy EA (2000) A performance measure of the degree of hand preference. Brain Cogn 44(3):402–414.  https://doi.org/10.1006/brcg.1999.1201 CrossRefPubMedGoogle Scholar
  8. Calvert GA, Bishop DVM (1998) Quantifying hand preference using a behavioural continuum. Laterality 3(3):255–268CrossRefGoogle Scholar
  9. Carson RG, Chua R, Goodman D, Byblow WD, Elliott D (1995) The preparation of aiming movements. Brain Cogn 28(2):133–154.  https://doi.org/10.1006/brcg.1995.1161 CrossRefPubMedGoogle Scholar
  10. Coelho CJ, Przybyla A, Yadav V, Sainburg RL (2013) Hemispheric differences in the control of limb dynamics: a link between arm performance asymmetries and arm selection patterns. J Neurophysiol 109(3):825–838.  https://doi.org/10.1152/jn.00885.2012 CrossRefPubMedGoogle Scholar
  11. Doyen AL, Duquenne V, Nuques S, Carlier M (2001) What can be learned from a lattice analysis of a laterality questionnaire? Behav Genet 31(2):193–207CrossRefGoogle Scholar
  12. Fagard J (2013) The nature and nurture of human infant hand preference. Ann Ny Acad Sci 1288(1):114–123.  https://doi.org/10.1111/nyas.12051 CrossRefPubMedGoogle Scholar
  13. Faul F, Erdfelder E, Lang A-G, Buchner A (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39(2):175–191CrossRefGoogle Scholar
  14. Gabbard C (1998) Attentional stimuli and programming hand selection: a developmental perspective. Int J Neurosci 96(3/4):205CrossRefGoogle Scholar
  15. Gabbard C, Rabb C (2000) What determines choice of limb for unimanual reaching movements? J Gen Psychol 127(2):178–184.  https://doi.org/10.1080/00221300009598577 CrossRefPubMedGoogle Scholar
  16. Gabbard C, Helbig CR, Gentry V (2001) Lateralized effects on reaching by children. Dev Neuropsychol 19(1):41–51.  https://doi.org/10.1207/S15326942DN1901_4 CrossRefPubMedGoogle Scholar
  17. Gonzalez CLR, Flindall JW, Stone KD (2015) Hand preference across the lifespan: effects of end-goal, task nature, and object location. Front Psychol 5:1579.  https://doi.org/10.3389/fpsyg.2014.01579 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gurd JM, Schulz J, Cherkas L, Ebers GC (2006) Hand preference and performance in 20 pairs of monozygotic twins with discordant handedness. Cortex 42(6):934–945.  https://doi.org/10.1016/S0010-9452(08)70438-6 CrossRefPubMedGoogle Scholar
  19. Hill EL, Khanem F (2009) The development of hand preference in children: the effect of task demands and links with manual dexterity. Brain Cogn 71(2):99–107.  https://doi.org/10.1016/j.bandc.2009.04.006 CrossRefPubMedGoogle Scholar
  20. Johnstone LT, Carey DP (2016) Do left hand reaction time advantages depend on localising unpredictable targets? Exp Brain Res 234(12):3625–3632.  https://doi.org/10.1007/s00221-016-4758-6 CrossRefPubMedGoogle Scholar
  21. Kilshaw D, Annett M (1983) Right-and left-hand skill I: effects of age, sex, and hand preference showing superior skill in left-handers. Br J Psychol 74:253–268.  https://doi.org/10.1111/j.2044-8295.1983.tb01861.x CrossRefPubMedGoogle Scholar
  22. Kim SG, Ashe J, Hendrich K, Ellermann JM, Merkle H, Ugurbil K, Georgopoulos AP (1993) Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. Science (New York) 261(5121):615–617CrossRefGoogle Scholar
  23. Kingstone A, Enns JT, Mangun GR, Gazzaniga MS (1995) Guided visual search is a left-hemisphere process in split-brain patients. Psychol Sci 6(2):118–121.  https://doi.org/10.1111/j.1467-9280.1995.tb00317.x CrossRefGoogle Scholar
  24. Klöppel S, van Eimeren T, Glauche V, Vongerichten A, Münchau A, Frackowiak RSJ et al (2007) The effect of handedness on cortical motor activation during simple bilateral movements. NeuroImage 34(1):274–280.  https://doi.org/10.1016/j.neuroimage.2006.08.038 CrossRefPubMedGoogle Scholar
  25. Leconte P, Fagard J (2006) Which factors affect hand selection in children’s grasping in hemispace? Combined effects of task demand and motor dominance. Brain Cogn 60(1):88–93.  https://doi.org/10.1016/j.bandc.2005.09.009 CrossRefPubMedGoogle Scholar
  26. Liang J, Wilkinson K, Sainburg RL (2018) Is hand selection modulated by cognitive-perceptual load? Neuroscience 369:363–373.  https://doi.org/10.1016/j.neuroscience.2017.11.005 CrossRefPubMedGoogle Scholar
  27. Mamolo CM, Roy EA, Bryden PJ, Rohr LE (2004) The effects of skill demands and object position on the distribution of preferred hand reaches. Brain Cogn 55(2):349–351.  https://doi.org/10.1016/j.bandc.2004.02.041 CrossRefPubMedGoogle Scholar
  28. Mamolo CM, Roy EA, Bryden PJ, Rohr LE (2005) The performance of left-handed participants on a preferential reaching test. Brain Cogn 57(2):143–145.  https://doi.org/10.1016/j.bandc.2004.08.033 CrossRefPubMedGoogle Scholar
  29. Marzi CA, Bisiacchi P, Nicoletti R (1991) Is interhemispheric transfer of visuomotor information asymmetric? Evidence from a meta-analysis. Neuropsychologia 29(12):1163–1177.  https://doi.org/10.1016/0028-3932(91)90031-3 CrossRefPubMedGoogle Scholar
  30. Mayer-Johnson R (1992) The picture communication symbols. Mayer-Johnson, Solana BeachGoogle Scholar
  31. Mieschke PE, Elliott D, Helsen WF, Carson RG, Coull JA (2001) Manual asymmetries in the preparation and control of goal-directed movements. Brain Cogn 45(1):129–140.  https://doi.org/10.1006/brcg.2000.1262 CrossRefPubMedGoogle Scholar
  32. Oldfield RC (1971) The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9(1):97–113.  https://doi.org/10.1016/0028-3932(71)90067-4 CrossRefPubMedGoogle Scholar
  33. Pinheiro J, Bates D, DebRoy S, Sarkar D, Core Team R (2018) nlme: linear and nonlinear mixed effects models. R package version 3:1–137. https://CRAN.R-project.org/package=nlme. Accessed 28 July 2018
  34. Pool E-M, Rehme AK, Fink GR, Eickhoff SB, Grefkes C (2014) Handedness and effective connectivity of the motor system. NeuroImage 99:451–460.  https://doi.org/10.1016/j.neuroimage.2014.05.048 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Przybyla A, Good DC, Sainburg RL (2012) Dynamic dominance varies with handedness: reduced interlimb asymmetries in left-handers. Exp Brain Res 216(3):419–431.  https://doi.org/10.1007/s00221-011-2946-y CrossRefPubMedGoogle Scholar
  36. Przybyla A, Coelho CJ, Akpinar S, Kirazci S, Sainburg RL (2013) Sensorimotor performance asymmetries predict hand selection. Neuroscience 228:349–360.  https://doi.org/10.1016/j.neuroscience.2012.10.046 CrossRefPubMedGoogle Scholar
  37. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 25 July 2018
  38. Rosenbaum DA (1980) Human movement initiation: specification of arm, direction, and extent. J Exp Psychol Gen 109(4):444–474CrossRefGoogle Scholar
  39. Scharoun SM, Bryden PJ (2014) Hand preference, performance abilities, and hand selection in children. Front Psychol 5(82):1–15.  https://doi.org/10.3389/fpsyg.2014.00082 CrossRefGoogle Scholar
  40. Steenhuis RE, Bryden MP (1999) The relation between hand preference and hand performance: what you get depends on what you measure. Laterality 4(1):3–26CrossRefGoogle Scholar
  41. Stoloff RH, Taylor JA, Xu J, Ridderikhoff A, Ivry RB (2011) Effect of Reinforcement History on Hand Choice in an Unconstrained Reaching Task. Front Neurosci-Switz 5:41.  https://doi.org/10.3389/fnins.2011.00041 CrossRefGoogle Scholar
  42. van den Berg FE, Swinnen SP, Wenderoth N (2011) Involvement of the primary motor cortex in controlling movements executed with the ipsilateral hand differs between left- and right-handers. J Cogn Neurosci 23(11):3456–3469.  https://doi.org/10.1162/jocn_a_00018 CrossRefPubMedGoogle Scholar
  43. Velay J-L, Benoit-Dubrocard S (1999) Hemispheric asymmetry and interhemispheric transferin reaching programming. Neuropsychologia 37(8):895–903.  https://doi.org/10.1016/S0028-3932(98)00149-3 CrossRefPubMedGoogle Scholar
  44. Verstynen T, Diedrichsen J, Albert N, Aparicio P, Ivry RB (2005) Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. J Neurophysiol 93(3):1209–1222.  https://doi.org/10.1152/jn.00720.2004 CrossRefPubMedGoogle Scholar
  45. Wilkinson KM, McIlvane WJ (2013) Perceptual factors influence visual search for meaningful symbols in individuals with intellectual disabilities and down syndrome or autism spectrum disorders. Ajidd-Am J Intellect 118(5):353–364.  https://doi.org/10.1352/1944-7558-118.5.353 CrossRefGoogle Scholar
  46. Wilkinson KM, O’Neill T, McIlvane WJ (2014) Eye-tracking measures reveal how changes in the design of aided aac displays influence the efficiency of locating symbols by school-age children without disabilities. J Speech Lang Hear R 57(2):455–466.  https://doi.org/10.1044/2013_JSLHR-L-12-0159 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Jiali Liang
    • 1
  • Krista M. Wilkinson
    • 1
    • 3
  • Robert L. Sainburg
    • 2
  1. 1.Department of Communication Sciences and DisordersThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of Kinesiology and NeurologyThe Pennsylvania State UniversityUniversity ParkUSA
  3. 3.E. K. Shriver Center of the University of Massachusetts Medical SchoolWorcesterUSA

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