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Executive Functions and Their Relation to Sleep Following Mild Traumatic Brain Injury in Preschoolers

Published online by Cambridge University Press:  16 August 2018

Catherine Landry-Roy ,
Annie Bernier ,
Jocelyn Gravel  and
Miriam H. Beauchamp
Catherine Landry-Roy
Affiliation:
Department of Psychology, University of Montreal, Quebec, Canada CHU Sainte-Justine Research Center, Montreal, Quebec, Canada
Annie Bernier
Affiliation:
Department of Psychology, University of Montreal, Quebec, Canada
Jocelyn Gravel
Affiliation:
Department of Psychology, University of Montreal, Quebec, Canada CHU Sainte-Justine Research Center, Montreal, Quebec, Canada
Miriam H. Beauchamp*
Affiliation:
Department of Psychology, University of Montreal, Quebec, Canada CHU Sainte-Justine Research Center, Montreal, Quebec, Canada
*
Correspondence and reprint requests to: Miriam H. Beauchamp, Department of Psychology, University of Montreal, C.P. 6128, Succursale Centre-Ville, Montreal, Quebec, Canada, H3C 3J7. E-mail: miriam.beauchamp@umontreal.ca
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Abstract

Objectives: Traumatic brain injury (TBI) sustained during childhood is known to impact children’s executive functioning. However, few studies have focused specifically on executive functioning after preschool TBI. TBI has also been associated with sleep disturbances, which are known to impair executive functions in healthy children. The aim of this study was to investigate executive functions in preschoolers with mild TBI, and to determine the role of sleep in the links between TBI and executive functioning. Methods: The sample was drawn from a longitudinal study and included 167 children, aged 18 to 60 months, divided into 2 groups: children with accidental mild TBI (n=84) and typically developing children (n=83). Children were assessed 6 months post-injury on executive function measures (inhibition and cognitive flexibility) and sleep measures (actigraphy data and parental rating of sleep problems). Results: The two groups did not differ in their executive abilities. However, relative to controls, children with mild TBI and shorter nighttime sleep duration or increased sleep problems exhibited poorer executive functions. Conclusions: These results support a “double hazard” effect, whereby the combination of sleep disturbances and mild TBI results in poorer executive functions. The findings highlight the importance of assessing and monitoring the quality of sleep even after mild head injuries. Poor sleep may place children at risk for increased cognitive difficulties. (JINS, 2018, 24, 769–780)

Keywords

Brain injuriesExecutive functionSleepChildCognitionPreschool
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 24 , Issue 8 , September 2018 , pp. 769 - 780
Copyright
Copyright © The International Neuropsychological Society 2018 

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References

REFERENCES

Acebo, C., Sadeh, A., Seifer, R., Tzischinsky, O., Wolfson, A.R., Hafer, A., &Carskadon, M.A. (1999). Estimating sleep patterns with activity monitoring in children and adolescents: How many nights are necessary for reliable measures? Sleep, 22, 95–103.Google Scholar
Achenbach, T.M., & Rescorla, L.A. (2001). Manual for the ASEBA school-age forms & profiles. Burlington, VT: University of Vermont, Research Center for Children Youth, & Families.Google Scholar
Alhola, P., & Polo-Kantola, P. (2007). Sleep deprivation: Impact on cognitive performance. Neuropsychiatric Disease and Treatment, 3, 553–567.Google Scholar
Anderson, P. (2002). Assessment and development of executive function (EF) during childhood. Child Neuropsychology, 8, 71–82.Google Scholar
Anderson, V. (1998). Assessing executive functions in children: Biological, psychological, and developmental considerations. Neuropsychological Rehabilitation, 8, 319–349.Google Scholar
Anderson, V., & Catroppa, C. (2005). Recovery of executive skills following paediatric traumatic brain injury (TBI): A 2 year follow-up. Brain Injury, 19, 459–470.Google Scholar
Asikainen, I., Kaste, M., & Sarna, S. (1996). Patients with traumatic brain injury referred to a rehabilitation and re-employment programme: Social and professional outcome for 508 Finnish patients 5 or more years after injury. Brain Injury, 10, 883–899.Google Scholar
Astill, R.G., Van der Heijden, K.B., Van Ijzendoorn, M.H., & Van Someren, E.J. (2012). Sleep, cognition, and behavioral problems in school-age children: A century of research meta-analyzed. Psychological Bulletin, 138, 1109–1138.Google Scholar
Beauchamp, M., Catroppa, C., Godfrey, C., Morse, S., Rosenfeld, J.V., & Anderson, V. (2011). Selective changes in executive functioning ten years after severe childhood traumatic brain injury. Developmental Neuropsychology, 36, 578–595.Google Scholar
Beauchamp, M.H., Landry-Roy, C., Gravel, J., Beaudoin, C., & Bernier, A. (2017). Should young children with TBI be compared with community or orthopedic control participants? Journal of Neurotrauma, 34, 2545–2552.Google Scholar
Beck, D.M., Schaefer, C., Pang, K., & Carlson, S.M. (2011). Executive function in preschool children: Test-retest reliability. Journal of Cognition and Development, 12, 169–193.Google Scholar
Becker, S.P., Ramsey, R.R., & Byars, K.C. (2015). Convergent validity of the Child Behavior Checklist sleep items with validated sleep measures and sleep disorder diagnoses in children and adolescents referred to a sleep disorders center. Sleep Medicine, 16, 79–86.Google Scholar
Bélanger, M.E., Bernier, A., Paquet, J., Simard, V., & Carrier, J. (2013). Validating actigraphy as a measure of sleep for preschool children. Journal of Clinical Sleep Medicine, 9, 701–706.Google Scholar
Bélanger, M.E., Bernier, A., Simard, V., Desrosiers, K., & Carrier, J. (2018). Sleeping toward behavioral regulation: Relations between sleep and externalizing symptoms in toddlers and preschoolers. Journal of Clinical Child & Adolescent Psychology, 47, 366–373.Google Scholar
Bélanger, M.E., Simard, V., Bernier, A., & Carrier, J. (2014). Investigating the convergence between actigraphy, maternal sleep diaries, and the Child Behavior Checklist as measures of sleep in toddlers. Frontiers in Psychiatry, 5, 158.Google Scholar
Bellerose, J., Bernier, A., Beaudoin, C., Gravel, J., & Beauchamp, M.H. (2015). When injury clouds understanding of others: Theory of mind after mild TBI in preschool children. Journal of the International Neuropsychological Society, 21, 483–493.Google Scholar
Bellerose, J., Bernier, A., Beaudoin, C., Gravel, J., & Beauchamp, M.H. (2017). Long-term brain-injury-specific effects following preschool mild TBI: A study of theory of mind. Neuropsychology, 31, 229–241.Google Scholar
Benington, J.H., & Frank, M.G. (2003). Cellular and molecular connections between sleep and synaptic plasticity. Progress in Neurobiology, 69, 71–101.Google Scholar
Bernier, A., Beauchamp, M.H., Bouvette-Turcot, A.A., Carlson, S.M., & Carrier, J. (2013). Sleep and cognition in preschool years: Specific links to executive functioning. Child Development, 84, 1542–1553.Google Scholar
Bernier, A., Carlson, S.M., Bordeleau, S., & Carrier, J. (2010). Relations between physiological and cognitive regulatory systems: Infant sleep regulation and subsequent executive functioning. Child Development, 81, 1739–1752.Google Scholar
Blishen, B.R., Carroll, W.K., & Moore, C. (1987). The 1981 socioeconomic index for occupations in Canada. Canadian Review of Sociology and Anthropology, 24, 465–488.Google Scholar
Byars, K.C., Yeomans-Maldonado, G., & Noll, J.G. (2011). Parental functioning and pediatric sleep disturbance: An examination of factors associated with parenting stress in children clinically referred for evaluation of insomnia. Sleep Medicine, 12, 898–905.Google Scholar
Carlson, S.M. (2005). Developmentally sensitive measures of executive function in preschool children. Developmental Neuropsychology, 28, 595–616.Google Scholar
Carlson, S.M., Davis, A.C., & Leach, J.G. (2005). Less is more: Executive function and symbolic representation in preschool children. Psychological Science, 16, 609–616.Google Scholar
Cassidy, J.D., Carroll, L.J., Peloso, P.M., Borg, J., von Holst, H., Holm, L., & Coronado, V.G. (2004). Incidence, risk factors and prevention of mild traumatic brain injury: Results of the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. Journal of Rehabilitation Medicine, 28–60.Google Scholar
Catroppa, C., Anderson, V.A., Morse, S.A., Haritou, F., & Rosenfeld, J.V. (2007). Children’s attentional skills 5 years post-TBI. Journal of Pediatric Psychology, 32, 354–369.Google Scholar
Collins, A., & Koechlin, E. (2012). Reasoning, learning, and creativity: Frontal lobe function and human decision-making. PLoS Biology, 10, e1001293.Google Scholar
Crowe, L., Babl, F., Anderson, V., & Catroppa, C. (2009). The epidemiology of paediatric head injuries: Data from a referral centre in Victoria, Australia. Journal of Paediatrics and Child Health, 45, 346–350.Google Scholar
Crowe, L.M., Catroppa, C., Babl, F.E., & Anderson, V. (2013). Executive function outcomes of children with traumatic brain injury sustained before three years. Child Neuropsychology, 19, 113–126.Google Scholar
Dahl, R.E. (1996). The regulation of sleep and arousal: Development and psychopathology. Development and Psychopathology, 8, 3–27.Google Scholar
Diamond, A. (2013). Executive functions. Annual Review Psycho!logy, 64, 135–168.Google Scholar
Durston, S., & Casey, B.J. (2006). What have we learned about cognitive development from neuroimaging? Neuropsychologia, 44, 2149–2157.Google Scholar
Ennis, E., & Henry, M. (2004). A review of social factors in the investigation and assessment of non-accidental head injury to children. Pediatric Rehabilitation, 7, 205–214.Google Scholar
Escalona, S.K. (1982). Babies at double hazard: Early development of infants at biologic and social risk. Pediatrics, 70, 670–676.Google Scholar
Ewing-Cobbs, L., Prasad, M.R., Landry, S.H., Kramer, L., & DeLeon, R. (2004). Executive functions following traumatic brain injury in young children: A preliminary analysis. Developmental Neuropsychology, 26, 487–512.Google Scholar
Friedman, N.P., Corley, R.P., Hewitt, J.K., & Wright, K.P., Jr. (2009). Individual differences in childhood sleep problems predict later cognitive executive control. Sleep, 32, 323–333.Google Scholar
Gagner, C., Landry-Roy, C., Bernier, A., Gravel, J., & Beauchamp, M.H. (2017). Behavioral consequences of mild traumatic brain injury in preschoolers. Psychological Medicine, Advance online publication. doi:10.1017/S0033291717003221 Google Scholar
Gagner, C., Landry-Roy, C., Laine, F., & Beauchamp, M.H. (2015). Sleep-wake disturbances and fatigue after pediatric traumatic brain injury: A systematic review of the literature. Journal of Neurotrauma, 32, 1539–1552.Google Scholar
Ganesalingam, K., Yeates, K.O., Taylor, H.G., Walz, N.C., Stancin, T., & Wade, S. (2011). Executive functions and social competence in young children 6 months following traumatic brain injury. Neuropsychology, 25, 466–476.Google Scholar
Garon, N., Bryson, S.E., & Smith, I.M. (2008). Executive function in preschoolers: A review using an integrative framework. Psychological Bulletin, 134, 31–60.Google Scholar
Goldberg, E., & Bougakov, D. (2005). Neuropsychologic assessment of frontal lobe dysfunction. The Psychiatric clinics of North America, 28, 567–580. 578–579.Google Scholar
Gregory, A.M., Caspi, A., Moffitt, T.E., & Poulton, R. (2009). Sleep problems in childhood predict neuropsychological functioning in adolescence. Pediatrics, 123, 1171–1176.Google Scholar
Gruber, R., Wiebe, S., Montecalvo, L., Brunetti, B., Amsel, R., & Carrier, J. (2011). Impact of sleep restriction on neurobehavioral functioning of children with attention deficit hyperactivity disorder. Sleep, 34, 315–323.Google Scholar
Harrison, Y., & Horne, J.A. (2000). Sleep loss and temporal memory. Quarterly Journal of Experimental Psychology, 53, 271–279.Google Scholar
Hawley, C.A., Ward, A.B., Long, J., Owen, D.W., & Magnay, A.R. (2003). Prevalence of traumatic brain injury amongst children admitted to hospital in one health district: A population-based study. Injury, 34, 256–260.Google Scholar
Horne, J.A. (1993). Human sleep, sleep loss and behaviour. Implications for the prefrontal cortex and psychiatric disorder. The British Journal of Psychiatry, 162, 413–419.Google Scholar
Ingvar, D.H. (1979). “Hyperfrontal” distribution of the cerebral grey matter flow in resting wakefulness; on the functional anatomy of the conscious state. Acta Neurologica Scandinavica, 60, 12–25.Google Scholar
Isquith, P.K., Crawford, J.S., Espy, K.A., & Gioia, G.A. (2005). Assessment of executive function in preschool-aged children. Mental Retardation and Developmental Disabilities Reasearch Reviews, 11, 209–215.Google Scholar
Jacobs, R., Harvey, A.S., & Anderson, V. (2007). Executive function following focal frontal lobe lesions: Impact of timing of lesion on outcome. Cortex, 43, 792–805.Google Scholar
Jones, K., & Harrison, Y. (2001). Frontal lobe function, sleep loss and fragmented sleep. Sleep Medicine Reviews, 5, 463–475.Google Scholar
Keenan, H.T., Runyan, D.K., Marshall, S.W., Nocera, M.A., & Merten, D.F. (2004). A population-based comparison of clinical and outcome characteristics of young children with serious inflicted and noninflicted traumatic brain injury. Pediatrics, 114, 633–639.Google Scholar
Kjellberg, A. (1977). Sleep deprivation and some aspects of performance: II. Lapses and other attentional effects. Waking & Sleeping, 1, 145–148.Google Scholar
Kochanska, G., Murray, K.T., & Harlan, E.T. (2000). Effortful control in early childhood: Continuity and change, antecedents, and implications for social development. Developmental Psychology, 36, 220–232.Google Scholar
Koslowsky, M., & Babkoff, H. (1992). Meta-analysis of the relationship between total sleep deprivation and performance. Chronobiology International, 9, 132–136.Google Scholar
Kreutzmann, J.C., Havekes, R., Abel, T., & Meerlo, P. (2015). Sleep deprivation and hippocampal vulnerability: Changes in neuronal plasticity, neurogenesis and cognitive function. Neuroscience, 309, 173–190.Google Scholar
Landry-Roy, C., Bernier, A., Gravel, J., & Beauchamp, M.H. (2017). Predictors of sleep outcomes following mild traumatic brain injury in preschoolers: Subjective and objective assessment of outcome. Journal of Head Trauma Rehabilitation, 32, E13–E23.Google Scholar
Lalonde, G., Bernier, A., Beaudoin, C., Gravel, J., & Beauchamp, M.H. (2016). Investigating social functioning after early mild TBI: The quality of parent–child interactions. Journal of Neuropsychology, 12, 1–22.Google Scholar
Levin, H.S., & Hanten, G. (2005). Executive functions after traumatic brain injury in children. Pediatric Neurology, 33, 79–93.Google Scholar
Lezak, M.D. (1982). The problem of assessing executive functions. International Journal of Psychology, 17, 281–297.Google Scholar
Loher, S., Fatzer, S.T., & Roebers, C.M. (2014). Executive functions after pediatric mild traumatic brain injury: A prospective short-term longitudinal study. Applied Neuropsychology: Child, 3, 103–114.Google Scholar
Mahmood, O., Rapport, L.J., Hanks, R.A., & Fichtenberg, N.L. (2004). Neuropsychological performance and sleep disturbance following traumatic brain injury. Journal of Head Trauma Rehabilitation, 19, 378–390.Google Scholar
Meerlo, P., Mistlberger, R.E., Jacobs, B.L., Heller, H.C., & McGinty, D. (2009). New neurons in the adult brain: The role of sleep and consequences of sleep loss. Sleep Medicine Reviews, 13, 187–194.Google Scholar
Meltzer, L.J., Walsh, C.M., Traylor, J., & Westin, A.M. (2012). Direct comparison of two new actigraphs and polysomnography in children and adolescents. Sleep, 35, 159–166.Google Scholar
Mittenberg, W., Wittner, M.S., & Miller, L.J. (1997). Postconcussion syndrome occurs in children. Neuropsychology, 11, 447–452.Google Scholar
Mustafa, A.G., & Alshboul, O.A. (2013). Pathophysiology of traumatic brain injury. Neurosciences, 18, 222–234.Google Scholar
Muzur, A., Pace-Schott, E.F., & Hobson, J.A. (2002). The prefrontal cortex in sleep. Trends in Cognitive Sciences, 6, 475–481.Google Scholar
Nadebaum, C., Anderson, V., & Catroppa, C. (2007). Executive function outcomes following traumatic brain injury in young children: A five year follow-up. Developmental Neuropsychology, 32, 703–728.Google Scholar
Nelson, T.D., Nelson, J.M., Kidwell, K.M., James, T.D., & Espy, K.A. (2015). Preschool sleep problems and differential associations with specific aspects of executive control in early elementary school. Developmental Neuropsychology, 40, 167–180.Google Scholar
Osmond, M.H., Klassen, T.P., Wells, G.A., Correll, R., Jarvis, A., Joubert, G., & Stiell, I.G. (2010). CATCH: A clinical decision rule for the use of computed tomography in children with minor head injury. Canadian Medical Association Journal, 182, 341–348.Google Scholar
Owens, J.A., Spirito, A., & McGuinn, M. (2000). The Children’s Sleep Habits Questionnaire (CSHQ): Psychometric properties of a survey instrument for school-aged children. Sleep, 23, 1043–1051.Google Scholar
Preacher, K.J., Curran, P.J., & Bauer, D.J. (2006). Computational tools for probing interactions in multiple linear regression, multilevel modeling, and latent curve analysis. Journal of Educational and Behavioral Statistics, 31, 437–448.Google Scholar
Randazzo, A.C., Muehlbach, M.J., Schweitzer, P.K., & Walsh, J.K. (1998). Cognitive function following acute sleep restriction in children ages 10–14. Sleep, 21, 861–868.Google Scholar
Sadeh, A. (2007). Consequences of sleep loss or sleep disruption in children. Sleep Medicine Clinics, 2, 513–520.Google Scholar
Sadeh, A. (2015). Sleep and development: Advancing theory and research: III. Sleep assessment methods. Monographs of the Society for Research in Child Development, 80, 33–48.Google Scholar
Sadeh, A., Gruber, R., & Raviv, A. (2002). Sleep, neurobehavioral functioning, and behavior problems in school-age children. Child Development, 73, 405–417.Google Scholar
Sadeh, A., Gruber, R., & Raviv, A. (2003). The effects of sleep restriction and extension on school-age children: What a difference an hour makes. Child Development, 74, 444–455.Google Scholar
Sazonov, E., Sazonova, N., Schuckers, S., & Neuman, M. (2004). Activity-based sleep-wake identification in infants. Physiological Measurement, 25, 1291–1304.Google Scholar
Scher, A., Hall, W.A., Zaidman-Zait, A., & Weinberg, J. (2010). Sleep quality, cortisol levels, and behavioral regulation in toddlers. Developmental Psychobiology, 52, 44–53.Google Scholar
Shay, N., Yeates, K.O., Walz, N.C., Stancin, T., Taylor, H.G., Beebe, D.W., & Wade, S.L. (2014). Sleep problems and their relationship to cognitive and behavioral outcomes in young children with traumatic brain injury. Journal of Neurotrauma, 31, 1305–1312.Google Scholar
Thurber, S., & Sheehan, W.P. (2012). Note on truncated T scores in discrepancy studies with the Child Behavior Checklist and Youth Self Report. Archives of Assessment Psychology, 2, 73–80.Google Scholar
Tsujimoto, S. (2008). The prefrontal cortex: Functional neural development during early childhood. The Neuroscientist, 14, 345–358.Google Scholar
Uttl, B. (2005). Measurement of individual differences: Lessons from memory assessment in research and clinical practice. Psychological Science, 16, 460–467.Google Scholar
Wang, L., Zhang, Z., McArdle, J.J., & Salthouse, T.A. (2009). Investigating ceiling effects in longitudinal data analysis. Multivariate Behavioral Research, 43, 476–496.Google Scholar
Ward, T.M., Gay, C., Alkon, A., Anders, T.F., & Lee, K.A. (2008). Nocturnal sleep and daytime nap behaviors in relation to salivary cortisol levels and temperament in preschool-age children attending child care. Biological Research for Nursing, 9, 244–253.Google Scholar
Wood, A.G., & Smith, E. (2008). Pediatric neuroimaging studies: A window to neurocognitive development of the frontal lobes. In V. Anderson, R. Jacobs & P.J. Anderson (Eds.), Executive functions and the frontal lobes (pp. 203–216). New York: Taylor & Francis.Google Scholar
Zelazo, P.D. (2006). The Dimensional Change Card Sort (DCCS): A method of assessing executive function in children. Nature Protocols, 1, 297–301.Google Scholar