Abstract
Drivers with neurodevelopmental disorders (NDDs), such as autism spectrum disorder (ASD) and attention-deficit/hyperactivity disorder (ADHD) are at increased risk of experiencing driving difficulties. An important aspect of driving safety and skill involves hazard detection. This functional magnetic resonance imaging study examined the neural responses associated with driving hazard detection in drivers with ASD, ADHD, and typically developing (TD) drivers. Forty participants (12 ASD, 15 ADHD, 13 TD) ages 16–30 years completed a driving simulator task in which they encountered social and nonsocial hazards; reaction time (RT) for responding to hazards was measured. Participants then completed a similar hazard detection task in the MRI scanner so that neural response to hazards could be measured. Activation of regions of interest considered part of the executive function (EF) and theory of mind (ToM) networks were examined and related to driving simulator behavior. Results showed that stronger activation of the EF network during social hazard processing, including the bilateral dorsolateral prefrontal cortex and posterior parietal cortex, was associated with faster RT to social hazards among drivers with ADHD, but not among drivers with ASD. This provides the first evidence of a relationship between EF network brain activation and driving skills in ADHD and suggests that alterations in this network may underlie driving behavior. In comparison, the current study did not observe a relationship between ToM network activation and RT to social hazards in any group. This study lays the groundwork for relating neural activation to driving behavior among individuals with NDDs.
Similar content being viewed by others
Data Availability
The datasets generated during and/or analyzed during the current study are not publicly available due to ongoing analysis of the data set but are available from the corresponding author on reasonable request.
References
AlAdawy D, Glazer M, Terwilliger J et al (2019) Eye contact between pedestrians and drivers. Proceedings of 2019 Driving Assessment Conference. https://arxiv.org/abs/1904.04188
Amano K, Goda N, Nishida S et al (2006) Estimation of the timing of human visual perception from magnetoencephalography. J Neurosci 26:3981–3991. https://doi.org/10.1523/JNEUROSCI.4343-05.2006
Ankem G, Klauer C, Ollendick T et al (2018) How risky are ADHD teen drivers? Analysis of ADHD teen drivers using naturalistic driving data. J Transp Health 9:S13. https://doi.org/10.1016/j.jth.2018.05.065
Arioli M, Canessa N (2019) Neural processing of social interaction: coordinate-based meta-analytic evidence from human neuroimaging studies. Hum Brain Mapp 40:3712–3737. https://doi.org/10.1002/hbm.24627
Barkley RA (1997) Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull 121:65–94. https://doi.org/10.1037/0033-2909.121.1.65
Barkley RA, Cox DJ (2007) A review of driving risks and impairments associated with attention-deficit/hyperactivity disorder and the effects of stimulant medication on driving performance. J Saf Res 38:113–128. https://doi.org/10.1016/j.jsr.2006.09.004
Barkley RA, Murphy KR (2011) The nature of executive function (EF) deficits in daily life activities in adults with ADHD and their relationship to performance on EF tests. J Psychopathol Behav Assess 33:137–158. https://doi.org/10.1007/s10862-011-9217-x
Barkley RA, Murphy KR, Kwasnik D (1996) Motor vehicle driving competencies and risks in teens and young adults with attention deficit hyperactivity disorder. Pediatrics 98:1089–1095
Barkley RA, Murphy KR, Dupaul GJ, Bush T (2002) Driving in young adults with attention deficit hyperactivity disorder: knowledge, performance, adverse outcomes, and the role of executive functioning. J Int Neuropsychol Soc 8:655–672. https://doi.org/10.1017/S1355617702801345
Baron-Cohen S (2001) Theory of mind and autism: a review. Spec Issues Int Rev Res Ment Retard 23:169–184. https://doi.org/10.1016/S0074-7750(00)80010-5
Baron-Cohen S, Leslie AM, Frith U (1985) Does the autistic child have a “theory of mind.” Cognition 21:37–46
Baron-Cohen S, Wheelwright S, Skinner R et al (2001) The autism spectrum quotient : evidence from Asperger syndrome/high functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord 31:5–17. https://doi.org/10.1023/A:1005653411471
Bednarz HM, Kana RK, Svancara AM et al (2021a) Neuropsychological predictors of driving hazard detection in autism spectrum disorder and ADHD. Child Neuropsychol 00:1–31. https://doi.org/10.1080/09297049.2021.1908531
Bednarz HM, Stavrinos D, Svancara AM et al (2021b) Behind the wheels with autism and ADHD: brain networks involved in driving hazard detection. Transp Res F: Traffic Psychol Behav 77:274–292. https://doi.org/10.1016/j.trf.2021.01.007
Beeli G, Koeneke S, Gasser K, Jancke L (2008) Brain stimulation modulates driving behavior. Behav Brain Funct 4:1–7. https://doi.org/10.1186/1744-9081-4-34
Biederman J, Fried R, Monuteaux MC et al (2007) A laboratory driving simulation for assessment of driving behavior in adults with ADHD: a controlled study. Ann Gen Psychiatry 6:1–7. https://doi.org/10.1186/1744-859X-6-4
Bishop H, Biasini FJ, Stavrinos D (2017) Social and non-social hazard response in drivers with autism spectrum disorder. J Autism Dev Disord 47:905–917. https://doi.org/10.1007/s10803-016-2992-1
Bishop H, Boe L, Stavrinos D, Mirman J (2018) Driving among adolescents with autism spectrum disorder and attention-deficit hyperactivity disorder. Safety 4:40
Bishop H, Curry AE, Stavrinos D, Mirman JH (2019) Characterizing the learning-to-drive period for teens with attention deficits. J Dev Behav Pediatr 40:581–588. https://doi.org/10.1097/DBP.0000000000000706
Borowsky A, Shinar D, Oron-Gilad T (2010) Age, skill, and hazard perception in driving. Accid Anal Prev 42:1240–1249. https://doi.org/10.1016/j.aap.2010.02.001
Brown B, Laurier E (2017) The trouble with autopilots: assisted and autonomous driving on the social road. Conf Hum Factors Comput Syst. https://doi.org/10.1145/3025453.3025462
Bruce CR, Unsworth CA, Dillon MP et al (2017) Hazard perception skills of young drivers with attention deficit hyperactivity disorder (ADHD) can be improved with computer based driver training: an exploratory randomised controlled trial. Accid Anal Prev 109:70–77. https://doi.org/10.1016/j.aap.2017.10.002
Canu WH, Stevens AE, Ranson L et al (2020) College readiness: differences between first-year undergraduates with and without ADHD. J Learn Disabil. https://doi.org/10.1177/0022219420972693
Chee DYT, Lee HC, Patomella AH, Falkmer T (2017) Driving behaviour profile of drivers with autism spectrum disorder (ASD). J Autism Dev Disord 47:2658–2670. https://doi.org/10.1007/s10803-017-3178-1
Chee DYT, Lee HCY, Patomella AH, Falkmer T (2019) Investigating the driving performance of drivers with and without autism spectrum disorders under complex driving conditions. Disabil Rehabil 41:1–8. https://doi.org/10.1080/09638288.2017.1370498
Christakou A, Murphy CM, Chantiluke K et al (2013) Disorder-specific functional abnormalities during sustained attention in youth with attention deficit hyperactivity disorder ( ADHD ) and with Autism. Mol Psychiatry. https://doi.org/10.1038/mp.2011.185
Cox SM, Cox DJ, Kofler MJ et al (2016) Driving simulator performance in novice drivers with autism spectrum disorder: the role of executive functions and basic motor skills. J Autism Dev Disord 46:1379–1391. https://doi.org/10.1007/s10803-015-2677-1
Cox DJ, Brown T, Ross V et al (2017) Can youth with autism spectrum disorder use virtual reality driving simulation training to evaluate and improve driving performance? An exploratory study. J Autism Dev Disord 47:2544–2555. https://doi.org/10.1007/s10803-017-3164-7
Craig F, Margari F, Legrottaglie AR et al (2016) A review of executive function deficits in autism spectrum disorder and attention-deficit/hyperactivity disorder. Neuropsychiatr Dis Treat 12:1191–1202. https://doi.org/10.2147/NDT.S104620
Crundall D, Chapman P, Trawley S et al (2012) Some hazards are more attractive than others: drivers of varying experience respond differently to different types of hazard. Accid Anal Prev. https://doi.org/10.1016/j.aap.2011.09.049
Curry AE, Metzger KB, Pfeiffer MR et al (2017) Motor vehicle crash risk among adolescents and young adults with attention-deficit/hyperactivity disorder. JAMA Pediatr 171:756–763. https://doi.org/10.1001/jamapediatrics.2017.0910
Curry AE, Yerys BE, Huang P, Metzger KB (2018) Longitudinal study of driver licensing rates among adolescents and young adults with autism spectrum disorder. Autism 22:479–488. https://doi.org/10.1177/1362361317699586
Curry AE, Yerys BE, Metzger KB et al (2019) Traffic crashes, violations, and suspensions among young drivers with ADHD. Pediatrics. https://doi.org/10.1542/peds.2018-2305
Daly BP, Nicholls EG, Patrick KE et al (2014) Driving behaviors in adults with autism spectrum disorders. J Autism Dev Disord 44:3119–3128. https://doi.org/10.1007/s10803-014-2166-y
Demetriou EA, Lampit A, Quintana DS et al (2018) Autism spectrum disorders: a meta-analysis of executive function. Mol Psychiatry 23:1198–1204. https://doi.org/10.1038/mp.2017.75
Demetriou EA, DeMayo MM, Guastella AJ (2019) Executive function in autism spectrum disorder: history, theoretical models, empirical findings, and potential as an endophenotype. Front Psychiatry 10:1–17. https://doi.org/10.3389/fpsyt.2019.00753
Drummond AE (2000) Paradigm lost! Paradise gained? An Australian’s perspective on novice driver safety. In: Novice Drivers Conference, 2000, Bristol, United Kingdom
Duncan AW, Bishop SL (2015) Understanding the gap between cognitive abilities and daily living skills in adolescents with autism spectrum disorders with average intelligence. Autism 19:64–72. https://doi.org/10.1177/1362361313510068
Elias R, White SW (2018) Autism goes to college: understanding the needs of a student population on the rise. J Autism Dev Disord 48:732–746. https://doi.org/10.1007/s10803-017-3075-7
Fuermaier ABM, Tucha L, Evans BL et al (2017) Driving and attention deficit hyperactivity disorder. J Neural Transm 124:55–67. https://doi.org/10.1007/s00702-015-1465-6
Garner AA, Gentry A, Welburn SC et al (2014) Symptom dimensions of disruptive behavior disorders in adolescent drivers. J Atten Disord 18:496–503. https://doi.org/10.1177/1087054711431699
Guéguen N, Meineri S, Eyssartier C (2015) A pedestrian’s stare and drivers’ stopping behavior: a field experiment at the pedestrian crossing. Saf Sci 75:87–89. https://doi.org/10.1016/j.ssci.2015.01.018
Guéguen N, Eyssartier C, Meineri S (2016) A pedestrian’s smile and drivers’ behavior: when a smile increases careful driving. J Saf Res 56:83–88. https://doi.org/10.1016/j.jsr.2015.12.005
Hawco C, Yoganathan L, Voineskos AN et al (2020) Greater individual variability in functional brain activity during working memory performance in young people with autism and executive function impairment. NeuroImage Clin 27:1–11. https://doi.org/10.1016/j.nicl.2020.102260
Horswill MS, Pachana NA, Wood J et al (2009) A comparison of the hazard perception ability of matched groups of healthy drivers aged 35 to 55, 65 to 74, and 75 to 84 years. J Int Neuropsychol Soc 15:799–802. https://doi.org/10.1017/S1355617709990312
Horswill MS, Anstey KJ, Hatherly CG, Wood JM (2010) The crash involvement of older drivers is associated with their hazard perception latencies. J Int Neuropsychol Soc 16:939–944. https://doi.org/10.1017/S135561771000055X
Huestegge L, Skottke EM, Anders S et al (2010) The development of hazard perception: dissociation of visual orientation and hazard processing. Transp Res F: Traffic Psychol Behav 13:1–8. https://doi.org/10.1016/j.trf.2009.09.005
Hull M (1992) Hazard perception test: the geelong trial and future development. In: National road safety seminar
Jensen AR (2006) Clocking the mind: mental chronometry and individual differences. Elsevier, Amsterdam
Jerome L, Habinski L, Segal A (2006) Attention-deficit/hyperactivity disorder (ADHD) and driving risk: a review of the literature and a methodological critique. Curr Psychiatry Rep 8:416–426. https://doi.org/10.1007/s11920-006-0045-8
Johnston K, Murray K, Spain D et al (2019) Executive function: cognition and behaviour in adults with autism spectrum disorders (ASD). J Autism Dev Disord 49:4181–4192. https://doi.org/10.1007/s10803-019-04133-7
Jonides J, Schumacher EH, Smith EE et al (1998) The role of parietal cortex in verbal working memory. J Neurosci 18:5026–5034. https://doi.org/10.1523/jneurosci.18-13-05026.1998
Kessler RC, Adler L, Ames M et al (2005) The World Health Organization adult ADHD self-report scale (ASRS): a short screening scale for use in the general population. Psychol Med 35:245–256. https://doi.org/10.1017/S0033291704002892
Kingery KM, Narad M, Garner AA et al (2015) Extended visual glances away from the roadway are associated with ADHD- and texting-related driving performance deficits in adolescents. J Abnorm Child Psychol 43:1175–1186. https://doi.org/10.1007/s10802-014-9954-x
Konstantopoulos P, Chapman P, Crundall D (2010) Driver’s visual attention as a function of driving experience and visibility. Using a driving simulator to explore drivers’ eye movements in day, night and rain driving. Accid Anal Prev 42:827–834. https://doi.org/10.1016/j.aap.2009.09.022
Lai CLE, Lau Z, Lui SSY et al (2017) Meta-analysis of neuropsychological measures of executive functioning in children and adolescents with high-functioning autism spectrum disorder. Autism Res 10:911–939. https://doi.org/10.1002/aur.1723
Mayhew DR, Simpson HM (1995) The role of experience: implications for the training and licensing of new drivers. Traffic Injury Research Foundation of Canada, Canada
McInerney K, Suhr J (2016) Neuropsychological correlates of hazard perception in older adults. J Int Neuropsychol Soc 22:332–340. https://doi.org/10.1017/S1355617715001253
McKenna FP, Crick JL (1994) Hazard perception in drivers: a methodology for testing and training. TRL Contract Rep. https://doi.org/10.13140/RG.2.1.3873.7766
Mckenna F, Crick J (1997) Developments in hazard perception prepared for road safety division, Department of the Environment, Transport and the Regions
Michaelis JR, McConnell DS, Smither JA (2012) Attention deficit/hyperactivity disorder’s effects on individuals’ scan paths during a simulated drive. Work 41:5833–5835. https://doi.org/10.3233/WOR-2012-0967-5833
National Highway Traffic Safety Administration (2018) Traffic safety facts (2016 data): young drivers. DOT HS 812(498):1–8
Ozonoff S, South M, Provencal S (2007) Executive functions in autism: theory and practice. New Dev Autism Futur Today. p 185–213
Panikratova YR, Vlasova RM, Akhutina TV et al (2020) Functional connectivity of the dorsolateral prefrontal cortex contributes to different components of executive functions. Int J Psychophysiol 151:70–79. https://doi.org/10.1016/j.ijpsycho.2020.02.013
Papagiannopoulou EA, Chitty KM, Hermens DF et al (2014) A systematic review and meta-analysis of eye-tracking studies in children with autism spectrum disorders. Soc Neurosci 9:610–632
Patrick KE, Hurewitz F, McCurdy MD et al (2018) Driving comparisons between young adults with autism spectrum disorder and typical development. J Dev Behav Pediatr 39:451–460
Patrick KE, Schultheis MT, Agate FT et al (2020) Executive function “drives” differences in simulated driving performance between young adults with and without autism spectrum disorder. Child Neuropsychol. https://doi.org/10.1080/09297049.2020.1713311
Peirce J, Gray JR, Simpson S et al (2019) PsychoPy2: experiments in behavior made easy. Behav Res Methods 51:195–203. https://doi.org/10.3758/s13428-018-01193-y
Pellicano E (2012) The development of executive function in autism. Autism Res Treat 2012:1–8. https://doi.org/10.1155/2012/146132
Poulsen AA, Horswill MS, Wetton MA et al (2010) A brief office-based hazard perception intervention for drivers with ADHD symptoms. Aust N Z J Psychiatry 44:528–534. https://doi.org/10.3109/00048671003596048
Quimby AR, Maycock G, Carter ID et al (1986) Perceptual abilities of accident involved drivers. J Saf Res. https://doi.org/10.1016/0022-4375(87)90068-5
Reimer B, Fried R, Mehler B et al (2013) Brief report: examining driving behavior in young adults with high functioning autism spectrum disorders: a pilot study using a driving simulation paradigm. J Autism Dev Disord 43:2211–2217. https://doi.org/10.1007/s10803-013-1764-4
Rösler L, End A, Gamer M (2017) Orienting towards social features in naturalistic scenes is reflexive. PLoS ONE 12:1–14. https://doi.org/10.1371/journal.pone.0182037
Ross V, Jongen EMM, Brijs K et al (2019) The relation between driving errors and executive functioning in intellectually able young novice drivers with autism. Transp Res F: Traffic Psychol Behav 63:38–54. https://doi.org/10.1016/j.trf.2019.03.003
Sakai H, Uchiyama Y, Tanaka S et al (2014) Prefrontal transcranial direct current stimulation improves fundamental vehicle control abilities. Behav Brain Res 273:57–62. https://doi.org/10.1016/j.bbr.2014.07.036
Salehinejad MA, Ghayerin E, Nejati V et al (2020) Domain-specific involvement of the right posterior parietal cortex in attention network and attentional control of ADHD: a randomized, cross-over, Sham-controlled tDCS study. Neuroscience 444:149–159. https://doi.org/10.1016/j.neuroscience.2020.07.037
Saxe R, Kanwisher N (2003) People thinking about thinking people: the role of the temporo-parietal junction in “theory of mind.” Neuroimage 19:1835–1842. https://doi.org/10.1016/S1053-8119(03)00230-1
Schurz M, Radua J, Aichhorn M et al (2014) Fractionating theory of mind: a meta-analysis of functional brain imaging studies. Neurosci Biobehav Rev 42:9–34. https://doi.org/10.1016/j.neubiorev.2014.01.009
Scialfa CT, Borkenhagen D, Lyon J et al (2012) The effects of driving experience on responses to a static hazard perception test. Accid Anal Prev 45:547–553. https://doi.org/10.1016/j.aap.2011.09.005
Seeley WW, Menon V, Schatzberg AF et al (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356. https://doi.org/10.1523/JNEUROSCI.5587-06.2007
Sheppard E, Ropar D, Underwood G, Van Loon E (2010) Brief report: driving hazard perception in autism. J Autism Dev Disord 40:504–508. https://doi.org/10.1007/s10803-009-0890-5
Sheppard E, van Loon E, Underwood G, Ropar D (2017) Attentional differences in a driving hazard perception task in adults with autism spectrum disorders. J Autism Dev Disord 47:405–414. https://doi.org/10.1007/s10803-016-2965-4
Smith SS, Horswill MS, Chambers B, Wetton M (2009) Hazard perception in novice and experienced drivers: the effects of sleepiness. Accid Anal Prev 41:729–733. https://doi.org/10.1016/j.aap.2009.03.016
Soltaninejad Z, Nejati V, Ekhtiari H (2015) Effect of anodal and cathodal transcranial direct current stimulation on DLPFC on modulation of inhibitory control in ADHD. J Atten Disord 23:325–332. https://doi.org/10.1177/1087054715618792
Stavrinos D, Mosley PR, Wittig SM et al (2016) Visual behavior differences in drivers across the lifespan: a digital billboard simulator study. Transp Res F: Traffic Psychol Behav 41:19–28. https://doi.org/10.1016/j.trf.2016.06.001
Sucha M, Dostal D, Risser R (2017) Pedestrian-driver communication and decision strategies at marked crossings. Accid Anal Prev 102:41–50. https://doi.org/10.1016/j.aap.2017.02.018
Team Rs (2015) RStudio: integrated development for R. RStudio, Inc, Boston, MA. http://www.rstudio.com. Accessed 28 Oct 2021
Ting Chee DY, Yeung Lee HC, Patomella AH, Falkmer T (2019) The visual search patterns of drivers with autism spectrum disorders in complex driving scenarios. J Transp Heal 14:100597. https://doi.org/10.1016/j.jth.2019.100597
Vaa T (2014) ADHD and relative risk of accidents in road traffic: a meta-analysis. Accid Anal Prev 62:415–425. https://doi.org/10.1016/j.aap.2013.10.003
van Dijk KRA, Sabuncu MR, Buckner RL (2012) The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 59:431–438. https://doi.org/10.1016/j.neuroimage.2011.07.044
van Veluw SJ, Chance SA (2014) Differentiating between self and others: an ALE meta-analysis of fMRI studies of self-recognition and theory of mind. Brain Imaging Behav 8:24–38. https://doi.org/10.1007/s11682-013-9266-8
Watts GR, Quimby AR (1979) Design and validation of a driving simulator. Rep LR 907
Wood G, Hartley G, Furley PA, Wilson MR (2016) Working memory capacity, visual attention and hazard perception in driving. J Appl Res Mem Cognit 5:454–462. https://doi.org/10.1016/j.jarmac.2016.04.009
Woodbury-Smith MR, Robinson J, Wheelwright S, Baron-Cohen S (2005) Screening adults for Asperger syndrome using the AQ: a preliminary study of its diagnostic validity in clinical practice. J Autism Dev Disord 35:331–335. https://doi.org/10.1007/s10803-005-3300-7
Yuval-Greenberg S, Keren A, Hilo R et al (2019) Gaze control during simulator driving in adolescents with and without attention deficit hyperactivity disorder. Am J Occup Ther 73:7303345030p1-7303345030p8
Acknowledgements
Special thanks to Piyush Pawar, MS for conducting data cleaning and preprocessing of driving simulator data, to Inaara Rajpari, BS for significant contributions to neuroimaging data collection, and to Edwin Cook, PhD for consultation regarding statistical analyses. The research described in this paper was supported by the Civitan International Pilot Research Grant, the University of Alabama College of Arts & Sciences Faculty Fund, and the University of Alabama at Birmingham Department of Psychology.
Funding
The research described in this paper was supported by the Civitan International Pilot Research Grant, the University of Alabama College of Arts & Sciences Faculty Fund, and the University of Alabama at Birmingham Department of Psychology.
Author information
Authors and Affiliations
Contributions
HB: Methodology, software, formal analysis, investigation, project administration, data curation, writing-original draft, writing-review & editing, visualization. DS: Conceptualization, methodology, resources, writing-review & editing, supervision, funding acquisition. AS: Software, investigation, project administration, data curation. GS: Investigation, project administration, data curation. BM: software, methodology, data curation. HD: Investigation. RK: Conceptualization, methodology resources, writing-review & editing, supervision, funding acquisition.
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that there is no conflict of interest.
Ethical Approval
This study was approved by the University’s Institutional Review Board (IRB). The study was performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendments.
Informed Consent
Informed consent was obtained from all subjects included in the study.
Additional information
Handling Editor: Micah M. Murray.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Bednarz, H.M., Stavrinos, D., Svancara, A.M. et al. Executive Function Brain Network Activation Predicts Driving Hazard Detection in ADHD. Brain Topogr 35, 251–267 (2022). https://doi.org/10.1007/s10548-021-00877-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10548-021-00877-7