Skip to main content Accessibility help
×
Home

Neurodevelopmental Outcomes and Neural Mechanisms Associated with Non-right Handedness in Children Born Very Preterm

  • Leona Pascoe (a1), Shannon E. Scratch (a1), Alice C. Burnett (a1) (a2) (a3), Deanne K. Thompson (a1) (a3) (a4), Katherine J. Lee (a3) (a5), Lex W. Doyle (a1) (a2) (a3) (a6), Jeanie L.Y. Cheong (a1) (a2) (a6), Terrie E. Inder (a7) and Peter J. Anderson (a1) (a3)...

Abstract

Non-right handedness (NRH) is reportedly more common in very preterm (VPT; <32 weeks’ gestation) children compared with term-born peers, but it is unclear whether neonatal brain injury or altered brain morphology and microstructure underpins NRH in this population. Given that NRH has been inconsistently reported to be associated with cognitive and motor difficulties, this study aimed to examine associations between handedness and neurodevelopmental outcomes in VPT 7-year-olds. Furthermore, the relationship between neonatal brain injury and integrity of motor tracts (corpus callosum and corticospinal tract) with handedness at age 7 years in VPT children was explored. One hundred seventy-five VPT and 69 term-born children completed neuropsychological and motor assessments and a measure of handedness at 7 years’ corrected age. At term-equivalent age, brain injury on MRI was assessed and diffusion tensor measures were obtained for the corpus callosum and posterior limb of the internal capsule. There was little evidence of stronger NRH in the VPT group compared with term controls (regression coefficient [b] −1.95, 95% confidence interval [−5.67, 1.77]). Poorer academic and working memory outcomes were associated with stronger NRH in the VPT group. While there was little evidence that neonatal unilateral brain injury was associated with stronger NRH, increased area and fractional anisotropy of the corpus callosum splenium were predictive of stronger NRH in the VPT group. VPT birth may alter the relationship between handedness and academic outcomes, and neonatal corpus callosum integrity predicts hand preference in VPT children at school age. (JINS, 2015, 21, 610–621)

Copyright

Corresponding author

Correspondence and reprint requests to: Leona Pascoe, Victorian Infant Brain Studies (VIBeS), Murdoch Childrens Research Institute, 50 Flemington Road, Parkville, Victoria 3052. +61 3 99366608 leona.pascoe@mcri.edu.au

References

Hide All
Adams, E., Chau, V., Poskitt, K.J., Grunau, R.E., Synnes, A., & Miller, S.P. (2010). Tractography-based quantitation of corticospinal tract development in premature newborns. The Journal of Pediatrics, 156(6), 882888, 888.e1. doi: 10.1016/j.jpeds.2009.12.030
Allin, M., Rooney, M., Griffiths, T., Cuddy, M., Wyatt, J., Rifkin, L., & Murray, R. (2006). Neurological abnormalities in young adults born preterm. Journal of Neurology, Neurosurgery, & Psychiatry, 77(4), 495499. doi: 10.1136/jnnp.2005.075465
Andrews, J.S., Ben-Shachar, M., Yeatman, J.D., Flom, L.L., Luna, B., & Feldman, H.M. (2010). Reading performance correlates with white-matter properties in preterm and term children. Developmental Medicine and Child Neurology, 52(6), e94e100. doi: 10.1111/j.1469-8749.2009.03456.x
Annett, M. (1967). The binomial distribution of right, mixed and left handedness. Quarterly Journal of Experimental Psychology, 19(4), 327333. doi: 10.1080/14640746708400109
Annett, M. (1985). Left, right, hand and brain: The right shift theory. London: Lawrence Erlbaum.
Bakan, P., Dibb, G., & Reed, P. (1973). Handedness and birth stress. Neuropsychologia, 11(3), 363366.
Briggs, G.G., & Nebes, R.D. (1975). Patterns of hand preference in a student population. Cortex, 11(3), 230238.
Caldu, X., Narberhaus, A., Junque, C., Gimenez, M., Vendrell, P., Bargallo, N., & Botet, F. (2006). Corpus callosum size and neuropsychologic impairment in adolescents who were born preterm. Journal of Child Neurology, 21(5), 406410.
Carlin, J.B., Gurrin, L.C., Sterne, J.A., Morley, R., & Dwyer, T. (2005). Regression models for twin studies: A critical review. International Journal of Epidemiology, 34(5), 10891099. doi: 10.1093/ije/dyi153
Cheong, J.L., Thompson, D.K., Wang, H.X., Hunt, R.W., Anderson, P.J., Inder, T.E., & Doyle, L.W. (2009). Abnormal white matter signal on MR imaging is related to abnormal tissue microstructure. AJNR: American Journal of Neuroradiology, 30(3), 623628. doi: 10.3174/ajnr.A1399
Constable, R.T., Ment, L.R., Vohr, B.R., Kesler, S.R., Fulbright, R.K., Lacadie, C., & Reiss, A.R. (2008). Prematurely born children demonstrate white matter microstructural differences at 12 years of age, relative to term control subjects: An investigation of group and gender effects. Pediatrics, 121(2), 306316. doi: 10.1542/peds.2007-0414
Coren, S., & Porac, C. (1980). Birth factors and laterality: Effects of birth order, parental age, and birth stress on four indices of lateral preference. Behavior Genetics, 10(2), 123138.
Domellof, E., Johansson, A.M., & Ronnqvist, L. (2011). Handedness in preterm born children: A systematic review and a meta-analysis. Neuropsychologia, 49(9), 22992310. doi: 10.1016/j.neuropsychologia.2011.04.033
Goodman, R. (1997). The strengths and difficulties questionnaire: A research note. Journal of Child Psychology and Psychiatry, 38(5), 581586.
Henderson, S.E., Sugden, D.A., & Barnett, A.L. (2007). Movement assessment battery for children-2: Movement ABC-2: Examiner’s manual. Delhi: Pearson.
Herve, P.Y., Crivello, F., Perchey, G., Mazoyer, B., & Tzourio-Mazoyer, N. (2006). Handedness and cerebral anatomical asymmetries in young adult males. Neuroimage, 29(4), 10661079. doi: 10.1016/j.neuroimage.2005.08.031
Herve, P.Y., Leonard, G., Perron, M., Pike, B., Pitiot, A., Richer, L., & Paus, T. (2009). Handedness, motor skills and maturation of the corticospinal tract in the adolescent brain. Human Brain Mapping, 30(10), 31513162. doi: 10.1002/hbm.20734
Heuchan, A.M., Evans, N., Henderson Smart, D.J., & Simpson, J.M. (2002). Perinatal risk factors for major intraventricular haemorrhage in the Australian and New Zealand Neonatal Network, 1995–97. Archives of Disease in Childhood. Fetal and Neonatal Edition, 86(2), F86F90. doi: 10.1136/fn.86.2.F86
Huppi, P.S., Murphy, B., Maier, S.E., Zientara, G.P., Inder, T.E., Barnes, P.D., & Volpe, J.J. (2001). Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics, 107(3), 455460.
Inder, T.E., Anderson, N.J., Spencer, C., Wells, S., & Volpe, J.J. (2003). White matter injury in the premature infant: A comparison between serial cranial sonographic and MR findings at term. AJNR. American Journal of Neuroradiology, 24(5), 805809.
Johnston, D.W., Nicholls, M.E., Shah, M., & Shields, M.A. (2009). Nature’s experiment? Handedness and early childhood development. Demography, 46(2), 281301.
Kesler, S.R., Vohr, B., Schneider, K.C., Katz, K.H., Makuch, R.W., Reiss, A.L., &Ment, L.R. (2006). Increased temporal lobe gyrification in preterm children. Neuropsychologia, 44(3), 445453. doi: http://dx.doi.org/10.1016/j.neuropsychologia.2005.05.015.
Kidokoro, H., Anderson, P.J., Doyle, L.W., Woodward, L.J., Neil, J.J., & Inder, T.E. (2014). Brain injury and altered brain growth in preterm infants: Predictors and prognosis. Pediatrics, 134(2), e444e453. doi: 10.1542/peds.2013-2336
Kidokoro, H., Neil, J.J., & Inder, T.E. (2013). New MR imaging assessment tool to define brain abnormalities in very preterm infants at term. AJNR: American Journal of Neuroradiology, 34(11), 22082214. doi: 10.3174/ajnr.A3521
Lancefield, K., Nosarti, C., Rifkin, L., Allin, M., Sham, P., & Murray, R. (2006). Cerebral asymmetry in 14 year olds born very preterm. Brain Research, 1093(1), 3340. doi: 10.1016/j.brainres.2006.03.097
Lawrence, E.J., Allen, G.M., Walshe, M., Allin, M., Murray, R., Rifkin, L.,& Nosarti, C. (2010). The corpus callosum and empathy in adults with a history of preterm birth. Journal of the International Neuropsychological Society, 16(4), 716720. doi: 10.1017/s1355617710000500
Luciana, M., Lindeke, L., Georgieff, M., Mills, M., & Nelson, C.A. (1999). Neurobehavioral evidence for working-memory deficits in school-aged children with histories of prematurity. Developmental Medicine and Child Neurology, 41(8), 521533.
Marlow, N., Hennessy, E.M., Bracewell, M.A., & Wolke, D. (2007). Motor and executive function at 6 years of age after extremely preterm birth. Pediatrics, 120(4), 793804. doi: 10.1542/peds.2007-0440
Marlow, N., Roberts, B.L., & Cooke, R.W. (1989). Laterality and prematurity. Archives of Disease in Childhood, 64(12), 17131716.
McManus, I.C. (1991). The inheritance of left-handedness. Ciba Foundation Symposium, 162, 251267; discussion, 267–281.
Medland, S.E., Duffy, D.L., Wright, M.J., Geffen, G.M., Hay, D.A., Levy, F., &Boomsma, D.I. (2009). Genetic influences on handedness: Data from 25,732 Australian and Dutch twin families. Neuropsychologia, 47(2), 330337.
Medland, S.E., Perelle, I., De Monte, V., & Ehrman, L. (2004). Effects of culture, sex, and age on the distribution of handedness: An evaluation of the sensitivity of three measures of handedness. Laterality, 9(3), 287297. doi: 10.1080/13576500342000040
Nicholls, M.E., Chapman, H.L., Loetscher, T., & Grimshaw, G.M. (2010). The relationship between hand preference, hand performance, and general cognitive ability. Journal of the International Neuropsychological Society, 16(4), 585592. doi: 10.1017/s1355617710000184
Nicholls, M.E., Johnston, D.W., & Shields, M.A. (2012). Adverse birth factors predict cognitive ability, but not hand preference. Neuropsychology, 26(5), 578587. doi: 10.1037/a0029151
Nosarti, C., Rushe, T.M., Woodruff, P.W., Stewart, A.L., Rifkin, L., & Murray, R.M. (2004). Corpus callosum size and very preterm birth: Relationship to neuropsychological outcome. Brain, 127(9), 20802089. doi: 10.1093/brain/awh230
O’Callaghan, M.J., Burn, Y.R., Mohay, H.A., Rogers, Y., & Tudehope, D.I. (1993). Handedness in extremely low birth weight infants: Aetiology and relationship to intellectual abilities, motor performance and behaviour at four and six years. Cortex, 29(4), 629637.
Omizzolo, C., Scratch, S.E., Stargatt, R., Kidokoro, H., Thompson, D.K., Lee, K.J., & Anderson, P.J. (2014). Neonatal brain abnormalities and memory and learning outcomes at 7 years in children born very preterm. Memory, 22(6), 605615. doi: 10.1080/09658211.2013.809765
Pickering, S., & Gathercole, S.E. (2001). Working memory test battery for children (WMTB-C). Lutz, FL: The Psychological Corporation.
Porac, C., & Coren, S. (1981). Lateral preferences and human behavior. New York: Springer.
Powls, A., Botting, N., Cooke, R.W.I., & Marlow, N. (1996). Handedness in very low birthweight (VLBW) children at 12 years of age: Relation to perinatal and outcome variables. Developmental Medicine & Child Neurology, 38(7), 594602. doi: 10.1111/j.1469-8749.1996.tb12124.x
Reidy, N., Morgan, A., Thompson, D.K., Inder, T.E., Doyle, L.W., & Anderson, P.J. (2013). Impaired language abilities and white matter abnormalities in children born very preterm and/or very low birth weight. The Journal of Pediatrics, 162(4), 719724. doi: 10.1016/j.jpeds.2012.10.017
Resch, F., Haffner, J., Parzer, P., Pfueller, U., Strehlow, U., & Zerahn-Hartung, C. (1997). Testing the hypothesis of the relationships between laterality and ability according to Annett’s right-shift theory: Findings in an epidemiological sample of young adults. British Journal of Psychology, 88(4), 621635.
Roberts, G., Howard, K., Spittle, A.J., Brown, N.C., Anderson, P.J., & Doyle, L.W. (2008). Rates of early intervention services in very preterm children with developmental disabilities at age 2 years. Journal of Paediatrics and Child Health, 44(5), 276280. doi: 10.1111/j.1440-1754.2007.01251.x
Roberts, G., Lim, J., Doyle, L.W., & Anderson, P.J. (2011). High rates of school readiness difficulties at 5 years of age in very preterm infants compared with term controls. Journal of Developmental and Behavioral Pediatrics, 32(2), 117124. doi: 10.1097/DBP.0b013e318206d5c9
Rodriguez, A., Kaakinen, M., Moilanen, I., Taanila, A., McGough, J.J., Loo, S., & Järvelin, M.-R. (2010). Mixed-handedness is linked to mental health problems in children and adolescents. Pediatrics, 125(2), e340e348.
Rodriguez, A., & Waldenström, U. (2008). Fetal origins of child non‐right‐handedness and mental health. Journal of Child Psychology and Psychiatry, 49(9), 967976.
Ross, G., Lipper, E., & Auld, P.A.M. (1992). Hand preference, prematurity and developmental outcome at school age. Neuropsychologia, 30(5), 483494.
Ross, G., Lipper, E.G., & Auld, P.A. (1987). Hand preference of four-year-old children: Its relationship to premature birth and neurodevelopmental outcome. Developmental Medicine and Child Neurology, 29(5), 615622.
Saigal, S., Rosenbaum, P., Szatmari, P., & Hoult, L. (1992). Non-right handedness among ELBW and term children at eight years in relation to cognitive function and school performance. Developmental Medicine & Child Neurology, 34(5), 425433. doi: 10.1111/j.1469-8749.1992.tb11455.x
Satz, P., Orsini, D.L., Saslow, E., & Henry, R. (1985). The pathological left-handedness syndrome. Brain and Cognition, 4(1), 2746. doi: http://dx.doi.org/10.1016/0278-2626(85)90052-1
Scharoun, S.M., & Bryden, P.J. (2014). Hand preference, performance abilities, and hand selection in children. Frontiers in Psychology, 5, 82. doi: 10.3389/fpsyg.2014.00082
Seizeur, R., Magro, E., Prima, S., Wiest-Daessle, N., Maumet, C., & Morandi, X. (2014). Corticospinal tract asymmetry and handedness in right- and left-handers by diffusion tensor tractography. Surgical and Radiologic Anatomy, 36(2), 111124. doi: 10.1007/s00276-013-1156-7
Semel, E., Wiig, E., & Secord, W. (2006). Clinical evaluation of language Fundamentals - Fourth edition, Australian standardised edition. Australia: Harcourt Assessment.
Shah, D.K., Doyle, L.W., Anderson, P.J., Bear, M., Daley, A.J., Hunt, R.W., & Inder, T.E. (2008). Adverse neurodevelopment in preterm infants with postnatal sepsis or necrotizing enterocolitis is mediated by white matter abnormalities on magnetic resonance imaging at term. The Journal of Pediatrics, 153(2), 170175.e1. doi: 10.1016/j.jpeds.2008.02.033
Skiöld, B., Horsch, S., Hallberg, B., Engström, M., Nagy, Z., Mosskin, M., & Ådén, U. (2010). White matter changes in extremely preterm infants, a population-based diffusion tensor imaging study. Acta Pædiatrica, 99(6), 842849. doi: 10.1111/j.1651-2227.2009.01634.x
Somers, M., Shields, L.S., Boks, M.P., Kahn, R.S., & Sommer, I.E. (2015). Cognitive benefits of right-handedness: A meta-analysis. Neuroscience and Biobehavioral Reviews, 51, 4863. doi: 10.1016/j.neubiorev.2015.01.003
StataCorp (2013). Stata Statistical Software: Release 13. College Station, TX: StataCorp LP.
Thompson, D.K., Inder, T.E., Faggian, N., Johnston, L., Warfield, S.K., Anderson, P.J.,& Egan, G.F. (2011). Characterization of the corpus callosum in very preterm and full-term infants utilizing MRI. Neuroimage, 55(2), 479490. doi: 10.1016/j.neuroimage.2010.12.025
Thompson, D.K., Inder, T.E., Faggian, N., Warfield, S.K., Anderson, P.J., Doyle, L.W., & Egan, G.F. (2012). Corpus callosum alterations in very preterm infants: Perinatal correlates and 2 year neurodevelopmental outcomes. Neuroimage, 59(4), 35713581. doi: 10.1016/j.neuroimage.2011.11.057
Thompson, D.K., Wood, S.J., Doyle, L.W., Warfield, S.K., Lodygensky, G.A., Anderson, P.J., & Inder, T.E. (2008). Neonate hippocampal volumes: Prematurity, perinatal predictors, and 2-year outcome. Annals of Neurology, 63(5), 642651. doi: 10.1002/ana.21367
Treyvaud, K., Ure, A., Doyle, L.W., Lee, K.J., Rogers, C.E., Kidokoro, H., & Anderson, P.J. (2013). Psychiatric outcomes at age seven for very preterm children: Rates and predictors. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 54(7), 772779. doi: 10.1111/jcpp.12040
Tuncer, M.C., Hatipoglu, E.S., & Ozates, M. (2005). Sexual dimorphism and handedness in the human corpus callosum based on magnetic resonance imaging. Surgical and Radiologic Anatomy, 27(3), 254259. doi: 10.1007/s00276-004-0308-1
Van der Elst, W., Hurks, P.P., Wassenberg, R., Meijs, C.J., Van Boxtel, M.P., & Jolles, J. (2011). On the association between lateral preferences and pregnancy/birth stress events in a nonclinical sample of school-aged children. Journal of Clinical and Expimental Neuropsychology, 33(1), 18. doi: 10.1080/13803391003757825
Wechsler, D. (1999). Wechsler abbreviated scale of intelligence. New York: The Psychological Corporation.
Welcome, S.E., Chiarello, C., Towler, S., Halderman, L.K., Otto, R., & Leonard, C.M. (2009). Behavioral correlates of corpus callosum size: Anatomical/behavioral relationships vary across sex/handedness groups. Neuropsychologia, 47(12), 24272435. doi: 10.1016/j.neuropsychologia.2009.04.008
Westerhausen, R., Huster, R.J., Kreuder, F., Wittling, W., & Schweiger, E. (2007). Corticospinal tract asymmetries at the level of the internal capsule: Is there an association with handedness? Neuroimage, 37(2), 379386. doi: 10.1016/j.neuroimage.2007.05.047
Westerhausen, R., Kreuder, F., Dos Santos Sequeira, S., Walter, C., Woerner, W., Wittling, R.A., & Wittling, W. (2004). Effects of handedness and gender on macro- and microstructure of the corpus callosum and its subregions: A combined high-resolution and diffusion-tensor MRI study. Brain Research: Cognitive Brain Research, 21(3), 418426. doi: 10.1016/j.cogbrainres.2004.07.002
Westerhausen, R., Walter, C., Kreuder, F., Wittling, R.A., Schweiger, E., & Wittling, W. (2003). The influence of handedness and gender on the microstructure of the human corpus callosum: A diffusion-tensor magnetic resonance imaging study. Neuroscience Letters, 351(2), 99102. doi: http://dx.doi.org/10.1016/j.neulet.2003.07.011
Wilkinson, G.S., & Robertson, G.J. (2006). WRAT 4: Wide Range Achievement Test - Professional manual. Lutz, Florida: Psychological Assessment Resources, Incorporated.
Wilson-Ching, M., Pascoe, L., Doyle, L.W., & Anderson, P.J. (2014). Effects of correcting for prematurity on cognitive test scores in childhood. Journal of Paediatrics and Child Health, 50(3), 182188. doi: 10.1111/jpc.12475
Wilson-Costello, D., Friedman, H., Minich, N., Siner, B., Taylor, G., Schluchter, M., & Hack, M. (2007). Improved neurodevelopmental outcomes for extremely low birth weight infants in 2000–2002. Pediatrics, 119(1), 3745. doi: 10.1542/peds.2006-1416
Witelson, S.F. (1985). The brain connection: The corpus callosum is larger in left-handers. Science, 229(4714), 665668.
Witelson, S.F. (1989). Hand and sex differences in the isthmus and genu of the human corpus callosum. A postmortem morphological study. Brain, 112(3), 799835.
Witelson, S.F., & Goldsmith, C.H. (1991). The relationship of hand preference to anatomy of the corpus callosum in men. Brain Research, 545(1-2), 175182.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed