Abstract
Sensorimotor timing deficits are considered central to attention-deficit/hyperactivity disorder (ADHD). However, the tasks establishing timing impairments often involve interconnected processes, including low-level sensorimotor timing and higher level executive processes such as attention. Thus, the source of timing deficits in ADHD remains unclear. Low-level sensorimotor timing can be isolated from higher level processes in a finger-tapping task that examines the motor response to unexpected shifts of metronome onsets. In this study, adults with ADHD and ADHD-like symptoms (n = 25) and controls (n = 26) performed two finger-tapping tasks. The first assessed tapping variability in a standard tapping task (metronome-paced and unpaced). In the other task, participants tapped along with a metronome that contained unexpected shifts (±15, 50 ms); the timing adjustment on the tap following the shift captures pre-attentive sensorimotor timing (i.e., phase correction) and thus should be free of potential higher order confounds (e.g., attention). In the standard tapping task, as expected, the ADHD group had higher timing variability in both paced and unpaced tappings. However, in the pre-attentive task, performance did not differ between the ADHD and control groups. Together, results suggest that low-level sensorimotor timing and phase correction are largely preserved in ADHD and that some timing impairments observed in ADHD may stem from higher level factors (such as sustained attention).
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References
Adler LA, Spencer T, Faraone SV (2006) Validity of pilot adult ADHD Self-Report Scale (ASRS) to rate adult ADHD symptoms. Ann Clin Psychiatry 18:145–148
Allman MJ, Meck WH (2012) Pathophysiological distortions in time perception and timed performance. Brain 135(3):656–677
Bailey JA, Penhune VB (2010) Rhythm synchronization performance and auditory working memory in early-and late-trained musicians. Exp Brain Res 204(1):91–101
Barnett V, Lewis T (1994) Outliers in statistical data, 3rd edn. Wiley, NY
Ben-Pazi H, Shalev RS, Gross-Tsur V, Bergman H (2006) Age and medication effects on rhythmic responses in ADHD: possible oscillatory mechanisms? Neuropsychologia 44:412–416
Castellanos FX, Tannock R (2002) Neuroscience of attention-deficit/hyperactivity disorder: the search for endophenotypes. Nat Rev Neurosci 3(8):617–628
Franklin MS, Mrazek MD, Anderson CL, Johnston C, Smallwood J, Kingstone A, Schooler JW (2014) Tracking distraction the relationship between mind-wandering, meta-awareness, and ADHD symptomatology. J Atten Disord. doi:10.1177/1087054714543494
Gilden DL, Marusich LR (2009) Contraction of time in attention-deficit hyperactivity disorder. Neuropsychology 23(2):265–269
Gomes H, Duff M, Flores A, Halperin JM (2013) Automatic processing of duration in children with attention-deficit/hyperactivity disorder. J Int Neuropyschol Soc 19:686–694
Grahn JA, Schuit D (2012) Individual differences in rhythmic ability: behavioral and neuroimaging investigations. PsychoMcol 22(2):105
Hervey AS, Epstein JN, Curry JF, Tonev S, Arnold LE, Conners CK, Hinshaw SP, Swanson JM, Hechtman L (2006) Reaction time distribution analysis of neuropsychological performance in an ADHD sample. Child Neuropsychol 12:125–140
Hove MJ, Keller PE (2015) Impaired movement timing in neurological disorders: rehabilitation and treatment strategies. Ann NY Acad Sci 1337(1):111–117
Hove MJ, Balasubramaniam R, Keller PE (2014a) The time course of phase correction: a kinematic investigation of motor adjustment to timing perturbations during sensorimotor synchronization. J Exp Psychol Hum Percept Perform 40:2243–2251
Hove MJ, Marie C, Bruce IC, Trainor LJ (2014b) Superior time perception for lower musical pitch explains why bass-ranged instruments lay down musical rhythms. Proc Natl Acad Sci USA 111(28):10383–10388
Hove MJ, Zeffiro TA, Biederman J, Li Z, Schmahmann J, Valera EM (2015) Postural sway and regional cerebellar volume in adults with attention-deficit/hyperactivity disorder. NeuroImage Clin 8:422–428
Huttunen T, Halonen A, Kaartinen J, Lyytinen H (2007) Does mismatch negativity show differences in reading-disabled children compared to normal children and children with attention deficit? Dev Neuropsychol 31(3):453–470
Huttunen-Scott T, Kaartinen J, Tolvanen A, Lyytinen H (2008) Mismatch negativity (MMN) elicited by duration deviations in children with reading disorder, attention deficit or both. Int J Psychophysiol 69(1):69–77
Ivry RB (1996) The representation of temporal information in perception and motor control. Curr Opin Neurobiol 6(6):851–857
Jacoby N, Tishby N, Repp BH, Ahissar M, Keller PE (2015) Parameter estimation of linear sensorimotor synchronization models: phase correction, period correction, and ensemble coordination. Timing Time Percept 3:52–87
Jacoby N, Tishby N, Jakoby H, Ahissar M (2016) Individual differences and reading skills: another PATH needed? In: 14th biennial international conference on music perception and cognition (ICMPC), San Francisco, CA. http://www.icmpc.org/icmpc14/files/ICMPC14_Proceedings.pdf. Accessed 31 Aug 2017
Kessler RC, Adler L, Ames M, Demler O, Faraone S, Hiripi E, Howes MJ, Jin R, Secnik K, Spencer T, Ustun TB, Walters EE (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
Kofler MJ, Rapport MD, Sarver DE, Raiker JS, Orban SA, Friedman LM, Kolomeyer EG (2013) Reaction time variability in ADHD: a meta-analytic review of 319 studies. Clin Psychol Rev 33:795–811
Kucyi A, Hove MJ, Biederman J, Van Dijk KR, Valera EM (2015) Disrupted functional connectivity of cerebellar default network areas in attention-deficit/hyperactivity disorder. Hum Brain Mapp 36(9):3373–3386
Kurdziel LBF, Dempsey K, Zahara M, Valera EM, Spencer RMC (2015) Impaired visuomotor adaptation in adults with ADHD. Exp Brain Res 233:1145–1153
Madison G, Merker B (2004) Human sensorimotor tracking of continuous subliminal deviations from isochrony. Neurosci Lett 370:69–73
Mates J (1994) A model of synchronization of motor acts to a stimulus sequence: I. timing and error corrections. Biol Cybern 70:463–473
Näätänen R, Paavilainen P, Rinne T, Alho K (2007) The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clin Neurophysiol 118(12):2544–2590
Noreika V, Falter CM, Rubia K (2013) Timing deficits in attention-deficit/hyperactivity disorder (ADHD): evidence from neurocognitive and neuroimaging studies. Neuropsychologia 51(2):235–266
Picton TW, Alain C, Otten L, Ritter W, Achim A (2000) Mismatch negativity: different water in the same river. Audiol Neurootol 5(3–4):111–139
Pressing J (1998) Error correction processes in temporal pattern production. J Math Psychol 42:63–101
Repp BH (2000) Compensation for subliminal timing perturbations in perceptual-motor synchronization. Psychol Res 63(2):106–128
Repp BH (2001) Phase correction, phase resetting, and phase shifts after subliminal timing perturbations in sensorimotor synchronization. J Exp Psychol Hum Percept Perform 27:600–621
Repp BH (2002) Automaticity and voluntary control of phase correction following event onset shifts in sensorimotor synchronization. J Exp Psychol Hum Percept Perform 28(2):410–430
Repp BH (2005) Sensorimotor synchronization: a review of the tapping literature. Psychon Bull Rev 12(6):969–992
Repp BH (2008) Perfect phase correction in synchronization with slow auditory sequences. J Motor Behav 40:363–367
Repp BH, Keller PE (2004) Adaptation to tempo changes in sensorimotor synchronization: effects of intention, attention, and awareness. Q J Exp Psychol A 57(3):499–521
Rommelse NN, Altink ME, Oosterlaan J, Beem L, Buschgens CJ, Buitelaar J, Sergeant JA (2008) Speed, variability, and timing of motor output in ADHD: which measures are useful for endophenotypic research? Behav Genet 38(2):121–132
Rubia K, Taylor A, Taylor E, Sergeant JA (1999) Synchronization, anticipation and consistency of motor timing in dimensionally defined children with attention deficit hyperactivity disorder. Percept Motor Skill 89:1237–1258
Rubia K, Noorloos J, Smith A, Gunning B, Sergeant J (2003) Motor timing deficits in community and clinical boys with hyperactive behavior: the effect of methylphenidate on motor timing. J Abnorm Child Psych 31:301–313
Schmiedek F, Oberauer K, Wilhelm O, Süb HM, Wittmann WW (2007) Individual differences in components of reaction time distributions and their relations to working memory and intelligence. J Exp Psychol Gen 136:414–429
Seli P, Cheyne JA, Smilek D (2013) Wandering minds and wavering rhythms: linking mind wandering and behavioral variability. J Exp Psychol Human 39(1):1–5
Semjen A, Vorberg D, Schulze HH (1998) Getting synchronized with the metronome: comparisons between phase and period correction. Psychol Res 61:44–55
Smith A, Taylor E, Warner-Rogers J, Newman S, Rubia K (2002) Evidence of a pure time perception deficit in children with ADHD. J Child Psychol Psychiatry 43:529–542
Thaut MH, Miller RA, Schauer LM (1998) Multiple synchronization strategies in rhythmic sensorimotor tasks: phase vs. period correction. Biol Cybern 79:241–250
Toplak ME, Tannock R (2005) Time perception: modality and duration effects in attention-deficit/hyperactivity disorder (ADHD). J Abnorm Child Psychol 33(5):639–654
Toplak ME, Rucklidge JJ, Hetherington R, John SCF, Tannock R (2003) Time perception deficits in attention-deficit/hyperactivity disorder and comorbid reading difficulties in child and adolescent samples. J Child Psychol Psychiatry 44:888–903
Toplak ME, Dockstader C, Tannock R (2006) Temporal information processing in ADHD: findings to date and new methods. J Neurosci Methods 151(1):15–29
Tukey J (1977) Exploratory data analysis. Addison-Wesley, Reading
Valera EM, Faraone SV, Murray K, Seidman LJ (2007) Meta-analysis of structural imaging findings in attention-deficit/hyperactivity disorder. Biol Psychiatry 61:1361–1369
Valera EM, Spencer RM, Zeffiro TA, Makris N, Spencer TJ, Faraone SV, Biederman J, Seidman LJ (2010) Neural substrates of impaired sensorimotor timing in adult attention-deficit/hyperactivity disorder. Biol Psychiatry 68(4):359–367
Wiener M, Turkeltaub P, Coslett HB (2010) The image of time: a voxel-wise meta analysis. Neuroimage 49(2):1728–1740
Willcutt EG, Doyle AE, Nigg JT, Faraone SV, Pennington BF (2005) Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol Psychiatry 57:1336–1346
Zelaznik HN, Vaughn AJ, Green JT, Smith AL, Hoza B, Linnea K (2012) Motor timing deficits in children with attention-deficit/hyperactivity disorder. Hum Mov Sci 31(1):255–265
Acknowledgements
We thank Laura Kurdziel for help recruiting participants and Heather Malone and Samantha Shorrock for help collecting data. This work was supported by grants from the National Institute of Health T32 MH16259 (to MJH) and R01 HD067744-01A1 (to EMV).
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Hove, M.J., Gravel, N., Spencer, R.M.C. et al. Finger tapping and pre-attentive sensorimotor timing in adults with ADHD. Exp Brain Res 235, 3663–3672 (2017). https://doi.org/10.1007/s00221-017-5089-y
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DOI: https://doi.org/10.1007/s00221-017-5089-y