Skip to main content Accessibility help
×
Home

Age-related grey matter volume correlates of response inhibition and shifting in attention-deficit hyperactivity disorder

  • Grainne M. McAlonan (a1), Vinci Cheung (a2), Siew E. Chua (a3), Jaap Oosterlaan (a4), Se-fong Hung (a5), Chun-pan Tang (a5), Chi-chiu Lee (a5), Shi-leung Kwong (a5), Ting-pong Ho (a6), Charlton Cheung (a6), John Suckling (a7) and Patrick W. L. Leung (a8)...

Abstract

Background

Children with attention-deficit hyperactivity disorder (ADHD) have difficulties with executive function and impulse control which may improve with age.

Aims

To map the brain correlates of executive function in ADHD and determine age-related changes in reaction times and brain volumes.

Method

Attention-deficit hyperactivity disorder and control groups were compared on the change task measures of response inhibition (stop signal reaction time, SSRT) and shifting (change response reaction time, CRRT). Voxel-wise magnetic resonance imaging (MRI) correlations of reaction times and grey matter volume were determined, along with bivariate correlations of reaction times, brain volumes and age.

Results

Individuals in the ADHD group had longer SSRTs and CRRTs. Anterior cingulate, striatal and medial temporal volumes highly correlated with SSRT. Striatal and cerebellar volumes strongly correlated with CRRT. Older children had faster reaction times and larger regional brain volumes. In controls, orbitofrontal, medial temporal and cerebellar volumes correlated with CRRT but not SSRT. Neither reaction times nor regional brain volumes were strongly age-dependent.

Conclusions

Our evidence supports delayed brain maturation in ADHD and implies that some features of ADHD improve with age.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Age-related grey matter volume correlates of response inhibition and shifting in attention-deficit hyperactivity disorder
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Age-related grey matter volume correlates of response inhibition and shifting in attention-deficit hyperactivity disorder
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Age-related grey matter volume correlates of response inhibition and shifting in attention-deficit hyperactivity disorder
      Available formats
      ×

Copyright

Corresponding author

Grainne M. McAlonan, Department of Psychiatry, University of Hong Kong, Pokfulam, Hong Kong. Email: mcalonan@hkucc.hku.hk

Footnotes

Hide All

Declaration of interest

None.

Funding detailed in Acknowledgements.

Footnotes

References

Hide All
1 Oosterlaan, J, Logan, GD, Sergeant, JA. Response inhibition in AD/HD, CD, comorbid AD/HD + CD, anxious, and control children: a meta-analysis of studies with the stop task. J Child Psychol Psychiatry 1998; 39: 411–25.
2 Lijffijt, M, Kenemans, JL, Verbaten, MN, van Engeland, H. A meta-analytic review of stopping performance in attention-deficit/hyperactivity disorder: deficient inhibitory motor control? J Abnorm Psychol 2005; 114: 216–22.
3 Oosterlaan, J, Sergeant, JA. Response inhibition and response re-engagement in attention-deficit/hyperactivity disorder, disruptive, anxious and normal children. Behav Brain Res 1998; 94: 3343.
4 Berger, A, Posner, MI. Pathologies of brain attentional networks. Neurosci Biobehav Rev 2000; 24: 35.
5 Shaw, P, Eckstrand, K, Sharp, W, Blumenthal, J, Lerch, JP, Greenstein, D, Clasen, L, Evans, A, Giedd, J, Rapoport, JL. Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc Natl Acad Sci USA 2007; 104: 19649–54.
6 Biederman, J, Mick, E, Faraone, SV. Age-dependent decline of symptoms of attention deficit hyperactivity disorder: impact of remission definition and symptom type. Am J Psychiatry 2000; 157: 816–8.
7 Carver, AC, Livesey, DJ, Charles, M. Age related changes in inhibitory control as measured by stop signal task performance. Int J Neurosci 2001; 107: 4361
8 McAlonan, GM, Cheung, V, Cheung, C, Chua, SE, Murphy, DG, Suckling, J, Tai, KS, Yip, LKC, Leung, P, Ho, TP. Mapping brain structure in attention deficit-hyperactivity disorder: a voxel-based MRI study of regional grey and white matter volume. Psychiatry Res 2007; 154: 171–80.
9 Wechsler, D. Wechsler Intelligence Scale for Children (3rd edn) (WISC–III). Psychological Corporation, 1992.
10 Ho, TP, Leung, PW, Lee, CC, Tang, CP, Hung, SF, Kwong, SL, Lucas, CP, Lieh-Mak, F, Shaffer, D. Test–retest reliability of the Chinese version of the Diagnostic Interview Schedule for Children–Version 4 (DISC–IV). J Child Psychol Psychiatry 2005; 46: 1135–8.
11 Tannock, R, Schachar, RJ, Carr, RP, Chajczyk, D, Logan, GD. Effects of methylphenidate on inhibitory control in hyperactive children. J Abnorm Child Psychol 1989; 17: 473–91.
12 Pallant, J. SPSS Survival Manual. A Step by Step Guide to Data Analysis Using SPSS: pp. 126–9. Open University Press, 2001.
13 Overmeyer, S, Bullmore, ET, Suckling, J, Simmons, A, Williams, SC, Santosh, PJ, Taylor, E. Distributed grey and white matter deficits in hyperkinetic disorder: MRI evidence for anatomical abnormality in an attentional network. Psychol Med 2001; 31: 1425–35.
14 Castellanos, FX, Giedd, JN, Eckburg, P, Marsh, WL, Vaituzis, AC, Kaysen, D, Hamburger, SD, Rapoport, JL. Quantitative morphology of the caudate nucleus in attention deficit hyperactivity disorder. Am J Psychiatry 1994; 151: 1791–6.
15 Seidman, LJ, Valera, EM, Makris, N, Monuteaux, MC, Boriel, DL, Kelkar, K, Kennedy, DN, Caviness, VS, Bush, G, Aleaedi, M, Faraone, SV, Bierderman, J. Dorsolateral prefrontal and anterior cingulate cortex volumetric abnormalities in adults with attention-deficit/hyperactivity disorder identified by magnetic resonance imaging. Biol Psychiatry 2006; 60: 1071–80.
16 Sowell, ER, Thompson, PM, Welcome, SE, Henkenius, AL, Toga, AW, Peterson, BS. Cortical abnormalities in children and adolescents with attention-deficit hyperactivity disorder. Lancet 2003; 362: 1699–707.
17 Mackie, S, Shaw, P, Lenroot, R, Pierson, R, Greenstein, DK, Nugent, TF, Sharp, WS, Giedd, JN, Rapoport, JL. Cerebellar development and clinical outcome in attention deficit hyperactivity disorder. Am J Psychiatry 2007; 164: 647–55.
18 Bush, G, Valera, EM, Seidman, LJ. Functional neuroimaging of attention-deficit/hyperactivity disorder: a review and suggested future directions. Biol Psychiatry 2005; 57: 1273–84.
19 Tamm, L, Menon, V, Ringel, J, Reiss, AL. Event-related FMRI evidence of frontotemporal involvement in aberrant response inhibition and task switching in attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 2004; 43: 1430–40.
20 Rubia, K, Overmeyer, S, Taylor, E, Brammer, M, Williams, SC, Simmons, A, Bullmore, ET. Hypofrontality in attention deficit hyperactivity disorder during higher-order motor control: a study with functional MRI. Am J Psychiatry 1999; 156: 891–6.
21 Schulz, KP, Fan, J, Tang, CY, Newcorn, JH, Buchsbaum, MS, Cheung, AM, Halperin, JM. Response inhibition in adolescents diagnosed with attention deficit hyperactivity disorder during childhood: an event-related FMRI study. Am J Psychiatry 2004; 161: 1650–7.
22 Dickstein, SG, Bannon, K, Castellanos, FX, Milham, MP. The neural correlates of attention deficit hyperactivity disorder: an ALE meta-analysis. J Child Psychol Psychiatry 2006; 47: 1051–62.
23 Casey, BJ, Castellanos, FX, Giedd, JN, Marsh, WL, Hamburger, SD, Schubert, AB, Vauss, YC, Vaituzis, AC, Dickstein, DP, Sarfatti, SE, Rapoport, JL. Implication of right frontostriatal circuitry in response inhibition and attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 1997; 36: 374–83.
24 Aron, AR, Dowson, JH, Sahakian, BJ, Robbins, TW. Methylphenidate improves response inhibition in adults with attention-deficit/hyperactivity disorder. Biol Psychiatry 2003; 54: 1465–8.
25 Aron, AR, Poldrack, RA. Cortical and subcortical contributions to Stop signal response inhibition: role of the subthalamic nucleus. J Neurosci 2006; 26: 2424–33.
26 Clark, L, Blackwell, AD, Aron, AR, Turner, DC, Dowson, J, Robbins, TW, Sahakian, BJ. Association between response inhibition and working memory in adult ADHD: a link to right frontal cortex pathology? Biol Psychiatry 2007; 61: 1395–401.
27 Middleton, FA, Strick, PL. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res 2000; 31: 236–50.
28 Middleton, FA, Strick, PL. Basal ganglia and cerebellar output influences non-motor function. Mol Psychiatry 1996; 1: 429–33.
29 Nosarti, C, Rubia, K, Smith, AB, Frearson, S, Williams, SC, Rifkin, L, Murray, RM. Altered functional neuroanatomy of response inhibition in adolescent males who were born very preterm. Dev Med Child Neurol 2006; 48: 265–71.
30 Vink, M, Ramsey, NF, Raemaekers, M, Kahn, RS. Striatal dysfunction in schizophrenia and unaffected relatives. Biol Psychiatry 2006; 60: 32–9.
31 Gothelf, D, Hoeft, F, Hinard, C, Hallmayer, JF, Stoecker, JVD, Antonarakis, SE, Morris, MA, Reiss, AL. Abnormal cortical activation during response inhibition in 22q11.2 deletion syndrome. Hum Brain Mapp 2007; 28: 533–42.
32 Nigg, JT. Is ADHD a disinhibitory disorder? Psychol Bull 2001; 127: 571–98.
33 Slusarek, M, Velling, S, Bunk, D, Eggers, C. Motivational effects on inhibitory control in children with ADHD. J Am Acad Child Adolesc Psychiatry 2001; 40: 355–63.
34 Gray, JA. Behavioural and neural-system analyses of the actions of anxiolytic drugs. Pharmacol Biochem Behav 1988; 29: 767–9.
35 Quay, HC. Inhibition and attention deficit hyperactivity disorder. J Abnorm Child Psychol 1997; 25: 713.
36 Tripp, G, Alsop, B. Sensitivity to reward frequency in boys with attention deficit hyperactivity disorder. J Clin Child Psychol 1999; 28: 366–75.
37 Luman, M, Oosterlaan, J, Sergeant, JA. The impact of reinforcement contingencies on AD/HD: a review and theoretical appraisal. Clin Psychol Rev 2005; 25: 183213.
38 Williams, ZM, Bush, G, Rauch, SL, Cosgrove, GR, Eskandar, EN. Human anterior cingulate neurons and the integration of monetary reward with motor responses. Nat Neurosci 2004; 7: 1370–5.
39 Bush, G, Luu, P, Posner, MI. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 2000; 4: 215–22.
40 McAlonan, GM, Cheung, V, Cheung, C, Suckling, J, Lam, GY, Tai, KS, Yip, L, Murphy, DGM, Chua, SE. Mapping the brain in autism. A voxel-based MRI study of volumetric differences and intercorrelations in autism. Brain 2005; 128: 268–76.
41 Barbas, H. Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices. Brain Res Bull 2000; 52: 319–30.
42 Swanson, JM, Flodman, P, Kennedy, J, Spence, MA, Moyzis, R, Schuck, S, Murias, M, Moriarity, J, Barr, C, Smith, M, Posner, M. Dopamine genes and ADHD. Neurosci Biobehav Rev 2000; 24: 21–5.
43 Giedd, JN, Blumenthal, J, Jeffries, NO, Castellanos, FX, Liu, H, Zijdenbos, A, Paus, T, Evans, AC, Rapoport, JL. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 1999; 2: 861–3.
44 Castellanos, FX, Lee, PP, Sharp, W, Jeffries, NO, Greenstein, DK, Clasen, LS, Blumenthal, JD, James, RS, Ebens, CL, Walter, JM, Zijdenbos, A, Evans, AC, Giedd, JN, Rapoport, JL. Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA 2002; 288: 1740–8.
45 Rosa-Neto, P, Lou, HC, Cumming, P, Pryds, O, Karrebaek, H, Lunding, J, Giedd, A. Methylphenidate-evoked changes in striatal dopamine correlate with inattention and impulsivity in adolescents with attention deficit hyperactivity disorder. NeuroImage 2005; 25: 868–76.

Age-related grey matter volume correlates of response inhibition and shifting in attention-deficit hyperactivity disorder

  • Grainne M. McAlonan (a1), Vinci Cheung (a2), Siew E. Chua (a3), Jaap Oosterlaan (a4), Se-fong Hung (a5), Chun-pan Tang (a5), Chi-chiu Lee (a5), Shi-leung Kwong (a5), Ting-pong Ho (a6), Charlton Cheung (a6), John Suckling (a7) and Patrick W. L. Leung (a8)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed

Age-related grey matter volume correlates of response inhibition and shifting in attention-deficit hyperactivity disorder

  • Grainne M. McAlonan (a1), Vinci Cheung (a2), Siew E. Chua (a3), Jaap Oosterlaan (a4), Se-fong Hung (a5), Chun-pan Tang (a5), Chi-chiu Lee (a5), Shi-leung Kwong (a5), Ting-pong Ho (a6), Charlton Cheung (a6), John Suckling (a7) and Patrick W. L. Leung (a8)...
Submit a response

eLetters

Putamen involvement in ADHD

Ian C Ellison-Wright, Consultant Psychiatrist
25 February 2009

We read with interest the study by McAlonan et al. (1) which found that in children with ADHD, slower reaction times in tests of attention were correlated with reduced gray matter in the right putamen. Evidence from several other sources implicates the putamen as having a central rolein the brain circuit mediating ADHD symptoms.

A study of ADHD symptoms in twenty-five children with focal stroke lesions found that the symptoms were most commonly associated with lesionsof the posterior putamen (2). Our meta-analysis of voxel-based MRI studieslocated the gray matter deficit in ADHD subjects in the right putamen/globus pallidus region (3). More recently, a study of basal ganglia shape found volume loss in parts of the putamen (bilaterally) in boys with ADHD (4).

The connectivity of the putamen can now be investigated by diffusion tensor imaging (5) and this may permit the identification of specific white matter tract changes in children with ADHD, providing a potential investigation to assist in earlier diagnosis.

References

1. McAlonan GM, Cheung V, Chua SE, Oosterlaan J, Hung SF, Tang CP, Lee CC, Kwong SL, Ho TP, Cheung C, Suckling J, Leung PW. Age-related grey matter volume correlates of response inhibition and shifting in attention-deficit hyperactivity disorder. Br J Psychiatry 2009;194:123-9.

2. Max JE, Fox PT, Lancaster JL, Kochunov P, Mathews K, Manes FF, Robertson BA, Arndt S, Robin DA, Lansing AE. Putamen lesions and the development of attention-deficit/hyperactivity symptomatology. J Am Acad Child Adolesc Psychiatry 2002; 41:563-71.

3. Ellison-Wright I, Ellison-Wright Z, Bullmore E. Structural brain change in Attention Deficit Hyperactivity Disorder identified by meta-analysis. BMC Psychiatry. 2008; 8:51.

4. Qiu A, Crocetti D, Adler M, Mahone EM, Denckla MB, Miller MI, Mostofsky SH. Basal ganglia volume and shape in children with attention deficit hyperactivity disorder. Am J Psychiatry 2009; 166:74-82.

5. Leh SE, Ptito A, Chakravarty MM, Strafella AP. Fronto-striatal connections in the human brain: a probabilistic diffusion tractography study. Neurosci Lett 2007; 419:113-8.
... More

Conflict of interest: None Declared

Write a reply

×

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *