Hostname: page-component-848d4c4894-cjp7w Total loading time: 0 Render date: 2024-06-13T21:44:01.503Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  02 September 2015

Leona Pascoe*
Clinical Sciences, Murdoch Childrens Research Institute, Melbourne, Australia
Shannon E. Scratch
Clinical Sciences, Murdoch Childrens Research Institute, Melbourne, Australia
Alice C. Burnett
Clinical Sciences, Murdoch Childrens Research Institute, Melbourne, Australia Premature Infant Follow-up Programme, Royal Women’s Hospital, Melbourne, Australia Department of Paediatrics, University of Melbourne, Melbourne, Australia
Deanne K. Thompson
Clinical Sciences, Murdoch Childrens Research Institute, Melbourne, Australia Department of Paediatrics, University of Melbourne, Melbourne, Australia Florey Institute of Neurosciences and Mental Health, Melbourne, Australia
Katherine J. Lee
Department of Paediatrics, University of Melbourne, Melbourne, Australia Clinical Epidemiology and Biostatistics Unit, Murdoch Childrens Research Institute, Melbourne, Australia
Lex W. Doyle
Clinical Sciences, Murdoch Childrens Research Institute, Melbourne, Australia Premature Infant Follow-up Programme, Royal Women’s Hospital, Melbourne, Australia Department of Paediatrics, University of Melbourne, Melbourne, Australia Department of Obstetrics and Gynaecology, Royal Women’s Hospital, Melbourne, Australia
Jeanie L.Y. Cheong
Clinical Sciences, Murdoch Childrens Research Institute, Melbourne, Australia Premature Infant Follow-up Programme, Royal Women’s Hospital, Melbourne, Australia Department of Obstetrics and Gynaecology, Royal Women’s Hospital, Melbourne, Australia
Terrie E. Inder
Department of Pediatric Newborn Medicine, Brigham and Women’s Hospital, Boston, United States
Peter J. Anderson
Clinical Sciences, Murdoch Childrens Research Institute, Melbourne, Australia Department of Paediatrics, University of Melbourne, Melbourne, Australia
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


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)

Research Articles
Copyright © The International Neuropsychological Society 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


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.2009.12.030CrossRefGoogle ScholarPubMed
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.2005.075465CrossRefGoogle ScholarPubMed
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.xCrossRefGoogle ScholarPubMed
Annett, M. (1967). The binomial distribution of right, mixed and left handedness. Quarterly Journal of Experimental Psychology, 19(4), 327333. doi: 10.1080/14640746708400109CrossRefGoogle ScholarPubMed
Annett, M. (1985). Left, right, hand and brain: The right shift theory. London: Lawrence Erlbaum.Google Scholar
Bakan, P., Dibb, G., & Reed, P. (1973). Handedness and birth stress. Neuropsychologia, 11(3), 363366.CrossRefGoogle ScholarPubMed
Briggs, G.G., & Nebes, R.D. (1975). Patterns of hand preference in a student population. Cortex, 11(3), 230238.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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/dyi153CrossRefGoogle ScholarPubMed
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.A1399CrossRefGoogle ScholarPubMed
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.2007-0414CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.2011.04.033CrossRefGoogle ScholarPubMed
Goodman, R. (1997). The strengths and difficulties questionnaire: A research note. Journal of Child Psychology and Psychiatry, 38(5), 581586.CrossRefGoogle ScholarPubMed
Henderson, S.E., Sugden, D.A., & Barnett, A.L. (2007). Movement assessment battery for children-2: Movement ABC-2: Examiner’s manual. Delhi: Pearson.Google Scholar
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.2005.08.031CrossRefGoogle ScholarPubMed
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.20734CrossRefGoogle ScholarPubMed
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.F86CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
Johnston, D.W., Nicholls, M.E., Shah, M., & Shields, M.A. (2009). Nature’s experiment? Handedness and early childhood development. Demography, 46(2), 281301.CrossRefGoogle ScholarPubMed
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: ScholarPubMed
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.2013-2336CrossRefGoogle ScholarPubMed
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.A3521CrossRefGoogle ScholarPubMed
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.2006.03.097CrossRefGoogle ScholarPubMed
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/s1355617710000500CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.2007-0440CrossRefGoogle ScholarPubMed
Marlow, N., Roberts, B.L., & Cooke, R.W. (1989). Laterality and prematurity. Archives of Disease in Childhood, 64(12), 17131716.CrossRefGoogle ScholarPubMed
McManus, I.C. (1991). The inheritance of left-handedness. Ciba Foundation Symposium, 162, 251267; discussion, 267–281.Google ScholarPubMed
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.CrossRefGoogle Scholar
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: 10.1080/13576500342000040CrossRefGoogle ScholarPubMed
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/s1355617710000184CrossRefGoogle ScholarPubMed
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/a0029151CrossRefGoogle Scholar
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/awh230CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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: 10.1080/09658211.2013.809765CrossRefGoogle ScholarPubMed
Pickering, S., & Gathercole, S.E. (2001). Working memory test battery for children (WMTB-C). Lutz, FL: The Psychological Corporation.Google Scholar
Porac, C., & Coren, S. (1981). Lateral preferences and human behavior. New York: Springer.CrossRefGoogle Scholar
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.xCrossRefGoogle ScholarPubMed
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.2012.10.017CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.xCrossRefGoogle Scholar
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.0b013e318206d5c9CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Rodriguez, A., & Waldenström, U. (2008). Fetal origins of child non‐right‐handedness and mental health. Journal of Child Psychology and Psychiatry, 49(9), 967976.CrossRefGoogle ScholarPubMed
Ross, G., Lipper, E., & Auld, P.A.M. (1992). Hand preference, prematurity and developmental outcome at school age. Neuropsychologia, 30(5), 483494.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.xCrossRefGoogle ScholarPubMed
Satz, P., Orsini, D.L., Saslow, E., & Henry, R. (1985). The pathological left-handedness syndrome. Brain and Cognition, 4(1), 2746. doi: ScholarPubMed
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.2014.00082CrossRefGoogle ScholarPubMed
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/s00276-013-1156-7CrossRefGoogle ScholarPubMed
Semel, E., Wiig, E., & Secord, W. (2006). Clinical evaluation of language Fundamentals - Fourth edition, Australian standardised edition. Australia: Harcourt Assessment.Google Scholar
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.2008.02.033CrossRefGoogle ScholarPubMed
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.xCrossRefGoogle ScholarPubMed
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.2015.01.003CrossRefGoogle ScholarPubMed
StataCorp (2013). Stata Statistical Software: Release 13. College Station, TX: StataCorp LP.Google Scholar
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.2010.12.025CrossRefGoogle ScholarPubMed
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.2011.11.057CrossRefGoogle ScholarPubMed
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.21367CrossRefGoogle ScholarPubMed
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.12040CrossRefGoogle ScholarPubMed
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/s00276-004-0308-1CrossRefGoogle ScholarPubMed
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: 10.1080/13803391003757825CrossRefGoogle Scholar
Wechsler, D. (1999). Wechsler abbreviated scale of intelligence. New York: The Psychological Corporation.Google Scholar
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.2009.04.008CrossRefGoogle Scholar
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.2007.05.047CrossRefGoogle ScholarPubMed
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.2004.07.002Google ScholarPubMed
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: ScholarPubMed
Wilkinson, G.S., & Robertson, G.J. (2006). WRAT 4: Wide Range Achievement Test - Professional manual. Lutz, Florida: Psychological Assessment Resources, Incorporated.Google Scholar
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.12475CrossRefGoogle ScholarPubMed
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.2006-1416CrossRefGoogle ScholarPubMed
Witelson, S.F. (1985). The brain connection: The corpus callosum is larger in left-handers. Science, 229(4714), 665668.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed