Elsevier

Neuropsychologia

Volume 99, May 2017, Pages 172-178
Neuropsychologia

Deficits in inhibitory force control in young adults with ADHD

https://doi.org/10.1016/j.neuropsychologia.2017.03.012Get rights and content

Highlights

  • Adults with and without ADHD completed a force-variant of the Go/No-Go task.

  • Adults with ADHD produced more force than adults without ADHD on failed inhibits.

  • The amount of force was a better predictor of ADHD compared to the standard task.

  • Precise and continuous motor tasks can be used to study behavioral deficits in ADHD.

Abstract

Poor inhibitory control is a well-established cognitive correlate of adults with ADHD. However, the simple reaction time (RT) task used in a majority of studies records performance errors only via the presence or absence of a single key press. This all-or-nothing response makes it impossible to capture subtle differences in underlying processes that shape performance. Subsequently, all-or-nothing tasks may underestimate the prevalence of executive function deficits in ADHD. The current study measured inhibitory control using a standard Go/No-Go RT task and a more sensitive continuous grip force task among adults with (N=51, 22 female) and without (N=51, 29 female) ADHD. Compared to adults without ADHD, adults with ADHD made more failed inhibits in the classic Go/No-Go paradigm and produced greater and more variable force during motor inhibition. The amount of force produced on failed inhibits was a stronger predictor of ADHD-related symptoms than the number of commissions in the standard RT task. Adults with ADHD did not differ from those without ADHD on the mean force and variability of force produced in Go trials. These findings suggest that the use of a precise and continuous motor task, such as the force task used here, provides additional information about the nature of inhibitory motor control in adults with ADHD.

Introduction

Attention deficit hyperactivity disorder (ADHD) is a common childhood-onset disorder characterized by age-inappropriate, chronic, pervasive, and impairing levels of inattention and/or hyperactivity-impulsivity (American Psychiatric Association 2013). ADHD persists into adulthood in up to 65% of cases (Faraone et al., 2006, Simon et al., 2009, Turgay et al., 2012), affects the ability to gain and maintain employment (Kessler et al., 2009, Kupper et al., 2012), and is associated with an increased risk for substance abuse (Wilens et al., 1995, Upadhyaya, 2008, Groenman et al., 2013), obesity (Cortese et al., 2008, Nazar et al., 2012, Nazar et al., 2014, Albayrak et al., 2013), workplace injuries (Swensen et al., 2004, Breslin and Pole, 2009, Hodgkins et al., 2011), and traffic accidents (Barkley et al., 1993, Jerome et al., 2006a, Jerome et al., 2006b, Barkley and Cox, 2007, Merkel et al., 2013). Though less often discussed, motor impairments are prominent among children with ADHD (Barkley, 1998) and up to 50% of pediatric ADHD patients are also comorbid for developmental coordination disorder (Kadesjo and Gillberg, 1999, Pitcher et al., 2003, Gillberg et al., 2004). Similarly, adults with ADHD have impaired visuomotor memory in gripping tasks (Neely et al., 2016), visuomotor adaptation in reaching tasks (Kurdziel et al., 2015), deficits in oculomotor control (Feifel et al., 2004, Carr et al., 2006), increased postural sway (Hove et al., 2015), and impaired timing in finger tapping tasks (Valera et al., 2010). These findings are important because motor processes have clearer neural correlates than many of the cognitive constructs associated with ADHD. Thus, the motor system provides a good avenue to examine the neurobiology of ADHD.

Inhibitory control is the process of suppressing competing responses to select the most appropriate response. The ability to suppress inappropriate behaviors in favor of appropriate alternatives is paramount to adapting behavior in changing circumstances and is thereby a critical component for controlling behavior at all levels, including movement. Although numerous studies report poor inhibitory control in ADHD (Nigg et al., 2002, Aron and Poldrack, 2005, Alderson et al., 2007, Wodka et al., 2007, Suskauer et al., 2008, Gilbert et al., 2011, Bari and Robbins, 2013), the type of task used in the majority of studies (e.g. go-no-go or stop signal reaction time, RT, task) records performance via the presence or absence of an all-or-nothing key press. Such an approach confounds cognitive, sensory, and motor processes into a single dichotomous response. As a result, we may be overlooking critical processes that provide insight into the neural mechanisms of the disorder. For example, a great deal of motor activity can be produced even when an individual does not ultimately press a key in a standard RT task. The current study overcomes this barrier by using a continuous and precise measure of motor output in a grip force variant of the classic go/no-go task. We used force output as a measure of activity in the motor system. In order to test the validity of this measure, participants completed a continuous grip force go/no-go task with both low and high force amplitude conditions as well as a standard go/no-go task that used an all-or-nothing keypress. Trials were presented rapidly, creating a prepotency to respond. In this context, the inhibition of a prepotent response requires effortful cognitive control, whereas allowing the motor response to proceed occurs in a more automatic fashion (Bargh et al., 1996, Muraven and Baumeister, 2000). We reasoned that greater activity in the motor system would be reflected by the production of larger forces during no-go trials. We included low and high force amplitude conditions as a means to examine response planning. In particular, the amount of force produced on a no-go trial may reflect a pre-planned response and scale to the target amplitude. Therefore, deficits in response planning would be indicated by force output (on no-go trials) that does not scale to the target amplitude.

Section snippets

Participants

We recruited young adults, ages 18–25, who identified as currently having ADHD or as having never been diagnosed with ADHD. Participants were community recruited through advertisements in State College, Pennsylvania. Exclusion criteria included: (1) previous concussions that resulted in a loss of consciousness for more than 10 min; (2) previous diagnosis of seizures, epilepsy, encephalitis, meningitis or an autism spectrum disorder; (3) previous diagnosis of a musculoskeletal or neurological

Participants

As reported in Table 1, independent univariate ANOVAs demonstrated that there were no differences in age or estimated IQ between the ADHD and control groups. The ADHD group reported significantly more ADHD-related symptoms in adulthood as measured by the CAADID and CAARS. As expected (Hinshaw et al., 2012, Anastopoulos et al., 2016), adults with ADHD self-reported more internalizing (e.g. anxiety or depression) and externalizing (e.g., aggression, rule-breaking behavior) difficulties on the ASR

Discussion

We report three novel findings. First, on Go trials of the force task, force output and variability was not different for adults with ADHD compared to adults without ADHD. Second, on No-Go trials in the force task, adults with ADHD produced greater and more variable force compared to adults without ADHD. Third, mean force output on No-Go trials was a stronger predictor of the CAARS S: L ADHD Index compared to performance in the standard RT task.

The lack of a group difference for force output

Conclusion

These current work represents a novel examination of inhibitory control in young adults. We demonstrated that the force variant of the Go/No-Go task is a precise and continuous measure of inhibitory control. As such, the resulting continuum of performance can be examined in relation to other behavioral, clinical, or physiological measures to provide greater information about the pathophysiology of inhibitory motor control. The results of the current study demonstrate that adults with ADHD have

Conflict of interest

The authors declare no competing financial interests.

Acknowledgements

This publication was supported, in part, by Grant UL1 TR002014 and KL2 TR002015 from the National Center for Advancing Translational Sciences (NCATS) to KAN. This publication was supported, in part, by Grant R01 MH084947 from the National institute for Mental Health (NIMH) to CHP. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

References (78)

  • C. Liston et al.

    Atypical prefrontal connectivity in attention-deficit/hyperactivity disorder: pathway to disease or pathological end point?

    Biol. Psychiatry

    (2011)
  • B.P. Nazar et al.

    Influence of attention-deficit/hyperactivity disorder on binge eating behaviors and psychiatric comorbidity profile of obese women

    Compr. Psychiatry

    (2014)
  • J. Prodoehl et al.

    Basal ganglia mechanisms underlying precision grip force control

    Neurosci. Biobehav Rev.

    (2009)
  • J.L. Reilly et al.

    Pharmacological treatment effects on eye movement control

    Brain Cogn.

    (2008)
  • L.J. Seidman et al.

    Structural brain imaging of attention-deficit/hyperactivity disorder

    Biol. Psychiatry

    (2005)
  • D.E. Vaillancourt et al.

    Subthalamic nucleus and internal globus pallidus scale with the rate of change of force production in humans

    Neuroimage

    (2004)
  • E.M. Valera et al.

    Neural substrates of impaired sensorimotor timing in adult attention-deficit/hyperactivity disorder

    Biol. Psychiatry

    (2010)
  • S.P. Wise et al.

    Motor aspects of cue-related neuronal activity in premotor cortex of the rhesus monkey

    Brain Res.

    (1983)
  • D.M. Wolpert et al.

    Internal models in the cerebellum

    Trends Cogn. Sci.

    (1998)
  • T.M.R., L.A. Achenbach

    Manual for the ASEBA Adult Forms and Profiles

    (2003)
  • O. Albayrak

    Common obesity risk alleles in childhood attention-deficit/hyperactivity disorder

    Am. J. Med. Genet. Part B, Neuropsychiatr. Genet.: Off. Publ. Int. Soc. Psychiatr. Genet.

    (2013)
  • R.M. Alderson et al.

    Attention-Deficit/Hyperactivity disorder and behavioral inhibition: a meta-analytic review of the stop-signal paradigm

    J. Abnorm Child Psych.

    (2007)
  • American Psychiatric Association., American Psychiatric Association. DSM-5 Task Force

    Diagnostic and statistical manual of mental disorders

    DSM-5

    (2013)
  • A.D. Anastopoulos et al.

    Rates and patterns of comorbidity among first-year college students with ADHD

    J. Clin. Child Adolesc. Psychol.

    (2016)
  • J.A. Bargh et al.

    Automaticity of social behavior: direct effects of trait construct and stereotype-activation on action

    J. Pers. Soc. Psychol.

    (1996)
  • R.A. Barkley

    Attention-deficit hyperactivity disorder

    Sci. Am.

    (1998)
  • R.A. Barkley et al.

    Driving-related risks and outcomes of attention deficit hyperactivity disorder in adolescents and young adults: a 3- to 5-year follow-up survey

    Pediatrics

    (1993)
  • L.W. Braud

    The effects of frontal EMG biofeedback and progressive relaxation upon hyperactivity and its behavioral concomitants

    Biofeedback and Self Regulation

    (1978)
  • F.C. Breslin et al.

    Work injury risk among young people with learning disabilities and attention-deficit/hyperactivity disorder in Canada

    Am. J. Public Health

    (2009)
  • L.A. Buddenberg et al.

    test-retest reliability of the purdue pegboard test

    Am. J. Occup. Ther.

    (2000)
  • L.A. Carr et al.

    Attentional versus motor inhibition in adults with attention-deficit/hyperactivity disorder

    Neuropsychology

    (2006)
  • S. Cortese et al.

    Toward systems neuroscience of ADHD: a meta-analysis of 55 fMRI studies

    Am. J. Psychiatry

    (2012)
  • S. Cortese et al.

    Attention-deficit/hyperactivity disorder (ADHD) and obesity: a systematic review of the literature

    Crit. Rev. Food Sci. Nutr.

    (2008)
  • S.V. Faraone et al.

    The age-dependent decline of attention deficit hyperactivity disorder: a meta-analysis of follow-up studies

    Psychol. Med.

    (2006)
  • F. Faul et al.

    Statistical power analyses using G*power 3.1: tests for correlation and regression analyses

    Behav. Res Methods

    (2009)
  • M. Favilla et al.

    Trajectory control in targeted force impulses. VII. Independent setting of amplitude and direction in response preparation

    Exp. Brain Res

    (1990)
  • D.L. Gilbert et al.

    Motor cortex inhibition: a marker of ADHD behavior and motor development in children

    Neurology

    (2011)
  • C. Gillberg et al.

    Co-existing disorders in ADHD – implications for diagnosis and intervention

    Eur. Child Adolesc. Psychiatry

    (2004)
  • A.P. Groenman et al.

    Substance use disorders in adolescents with attention deficit hyperactivity disorder: a 4-year follow-up study

    Addiction

    (2013)
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