Abstract
Background/objective
Inhibitory control, the ability to suppress prepotent responses and resist irrelevant stimuli, is thought to play a critical role in the manifestation and maintenance of obesity in adolescents. Adolescence is a unique developmental stage characterized by significant maturational changes in cortical structures (i.e., prefrontal cortex: PFC) that relate to inhibitory control processes. The current study investigated the behavioral and neurophysiological correlates of inhibitory control in adolescents with obesity.
Subjects/methods
We compared 18 normal-weight and 22 adolescents with obesity on performance and electroencephalography (EEG)-based measures during a Go/NoGo task. We investigated N2 and P3 event-related potential (ERP) components.
Results
Adolescents with obesity showed lower accuracy compared to their normal-weight peers in NoGo trials where greater amounts of inhibitory control effort were required (p = 0.03). Adolescents with obesity had larger NoGo N2 amplitude relative to the Go N2 amplitude (p = 0.03), whereas this difference was not observed in the healthy weight sample. Furthermore, a lower self-efficacy of individual’s ability to control eating behaviors in challenging situations (as measured by the Weight Efficacy Lifestyle-Short Form) directly correlated with larger NoGo N2 amplitudes for both obese (p = 0.03) and normal weight groups (p = 0.01).
Conclusions
These findings suggested that obesity in adolescence is associated with a decreased ability to modulate cognitive conflict during the inhibitory control processing. The individual differences in conflict monitoring during situations where greater amounts of inhibitory control effort were required might provide an explanation for overeating behaviors in obese adolescents.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Wang Y, Beydoun MA. The obesity epidemic in the United States—gender, age, socioeconomic, racial/ethnic, and geographic characteristics: a systematic review and meta-regression analysis. Epidemiol Rev. 2007;29:6–28.
Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011–2012. JAMA. 2014;311:806–14.
Hedley AA, Ogden CL, Johnson CL, Carroll MD, Curtin LR, Flegal KM. Prevalence of overweight and obesity among US children, adolescents, and adults, 1999–2002. JAMA. 2004;291:2847–50.
Griffiths LJ, Parsons TJ, Hill AJ. Self‐esteem and quality of life in obese children and adolescents: a systematic review. Pediatr Obes. 2010;5:282–304.
Smith E, Hay P, Campbell L, Trollor JN. A review of the association between obesity and cognitive function across the lifespan: implications for novel approaches to prevention and treatment. Obes Rev. 2011;12:740–55.
Woltering S, Lewis MD. Developmental pathways of emotion regulation in childhood: a neuropsychological perspective. Mind Brain Educ. 2009;3:160–9.
Barkley RA. The executive functions and self-regulation: an evolutionary neuropsychological perspective. Neuropsychol Rev. 2001;11:1–29.
Woltering S, Shi Q. On the neuroscience of self-regulation in children with disruptive behavior problems: implications for education. Rev Educ Res. 2016;86:1085–110.
Pauli-Pott U, Albayrak Ö, Hebebrand J, Pott W. Does inhibitory control capacity in overweight and obese children and adolescents predict success in a weight-reduction program? Eur Child Adolesc Psychiatry. 2010;19:135–41.
Anzman SL, Birch LL. Low inhibitory control and restrictive feeding practices predict weight outcomes. J Pediatr. 2009;155:651–6.
Gunstad J, Spitznagel MB, Paul RH, Cohen RA, Kohn M, Luyster FS, et al. Body mass index and neuropsychological function in healthy children and adolescents. Appetite. 2008;50:246–51.
Schunk DH, Ertmer PA. Self-regulation and academic learning: self-efficacy enhancing interventions. In: Handbook of self-regulation. Elsevier; 2000. p. 631–49.
Dennis KE, Goldberg AP. Weight control self-efficacy types and transitions affect weight-loss outcomes in obese women. Addict Behav. 1996;21:103–16.
Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD. The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: a latent variable analysis. Cogn Psychol. 2000;41:49–100.
Nigg JT. Neuropsychologic theory and findings in attention-deficit/hyperactivity disorder: the state of the field and salient challenges for the coming decade. Biol Psychiatry. 2005;57:1424–35.
Wulfert E, Block JA, Santa Ana E, Rodriguez ML, Colsman M. Delay of gratification: impulsive choices and problem behaviors in early and late adolescence. J Pers. 2002;70:533–52.
DePasque S, Galván A. Frontostriatal development and probabilistic reinforcement learning during adolescence. Neurobiol Learn Mem. 2017;143:1–7.
Bush G, Luu P, Posner MI. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci. 2000;4:215–22.
Chapman H, Woltering S, Lamm C, Lewis M. Hearts and minds: coordination of neurocognitive and cardiovascular regulation in children and adolescents. Biol Psychol. 2010;84:296–303.
Bokura H, Yamaguchi S, Kobayashi S. Electrophysiological correlates for response inhibition in a Go/NoGo task. Clin Neurophysiol. 2001;112:2224–32.
Falkenstein M. Inhibition, conflict and the Nogo-N2. Clin Neurophysiol. 2006;117:1638–40.
Jonkman LM. The development of preparation, conflict monitoring and inhibition from early childhood to young adulthood; a Go/Nogo ERP study. Brain Res. 2006;1097:181–93.
Folstein JR, Van Petten C. Influence of cognitive control and mismatch on the N2 component of the ERP: a review. Psychophysiology. 2008;45:152–70.
Falkenstein M, Hoormann J, Hohnsbein J. ERP components in Go/Nogo tasks and their relation to inhibition. Acta Psychol (Amst). 1999;101:267–91.
Nieuwenhuis S, Yeung N, Van Den Wildenberg W, Ridderinkhof KR. Electrophysiological correlates of anterior cingulate function in a go/no-go task: effects of response conflict and trial type frequency. Cogn Affect Behav Neurosci. 2003;3:17–26.
Bekker EM, Kenemans JL, Verbaten MN. Source analysis of the N2 in a cued Go/NoGo task. Cogn Brain Res. 2005;22:221–31.
Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S. The role of the medial frontal cortex in cognitive control. Science. 2004;306:443–7.
Watson TD, Garvey KT. Neurocognitive correlates of processing food-related stimuli in a Go/No-go paradigm. Appetite. 2013;71:40–7.
Blackburne T, Rodriguez A, Johnstone SJ. A serious game to increase healthy food consumption in overweight or obese adults: randomized controlled trial. JMIR Serious Games. 2016;4 (2).
Tarantino V, Vindigni V, Bassetto F, Pavan C, Vallesi A. Behavioral and electrophysiological correlates of cognitive control in ex-obese adults. Biol Psychol. 2017;127:198–208.
Kamijo K, Pontifex MB, Khan NA, Raine LB, Scudder MR, Drollette ES, et al. The association of childhood obesity to neuroelectric indices of inhibition. Psychophysiology. 2012;49:1361–71.
Jonkman L, Lansbergen M, Stauder J. Developmental differences in behavioral and event‐related brain responses associated with response preparation and inhibition in a go/nogo task. Psychophysiology. 2003;40:752–61.
Bruin K, Wijers A, Van Staveren A. Response priming in a go/nogo task: do we have to explain the go/nogo N2 effect in terms of response activation instead of inhibition? Clin Neurophysiol. 2001;112:1660–71.
Eimer M. Effects of attention and stimulus probability on ERPs in a Go/Nogo task. Biol Psychol. 1993;35:123–38.
Tascilar ME, Turkkahraman D, Oz O, Yucel M, Taskesen M, Eker I, et al. P300 auditory event‐related potentials in children with obesity: is childhood obesity related to impairment in cognitive functions? Pediatr Diabetes. 2011;12:589–95.
Reyes S, Peirano P, Peigneux P, Lozoff B, Algarin C. Inhibitory control in otherwise healthy overweight 10-year-old children. Int J Obes. 2015;39:1230.
Song T-F, Chi L, Chu C-H, Chen F-T, Zhou C, Chang Y-K. Obesity, cardiovascular fitness, and inhibition function: an electrophysiological study. Front Psychol. 2016;7:1124.
Junghöfer M, Elbert T, Leiderer P, Berg P, Rockstroh B. Mapping EEG-potentials on the surface of the brain: a strategy for uncovering cortical sources. Brain Topogr. 1997;9:203–17.
Olvet DM, Hajcak G. The stability of error‐related brain activity with increasing trials. Psychophysiology. 2009;46:957–61.
Junghöfer M, Elbert T, Tucker DM, Braun C. The polar average reference effect: a bias in estimating the head surface integral in EEG recording. Clin Neurophysiol. 1999;110:1149–55.
Liu Z-X, Lishak V, Tannock R, Woltering S. Effects of working memory training on neural correlates of Go/Nogo response control in adults with ADHD: a randomized controlled trial. Neuropsychologia. 2017;95:54–72.
Woltering S, Liu Z, Rokeach A, Tannock R. Neurophysiological differences in inhibitory control between adults with ADHD and their peers. Neuropsychologia. 2013;51:1888–95.
Davis EP, Bruce J, Snyder K, Nelson CA. The X-trials: neural correlates of an inhibitory control task in children and adults. J Cogn Neurosci. 2003;15:432–43.
Wiersema R, Van Der Meere J, Antrop I, Roeyers H. State regulation in adult ADHD: an event-related potential study. J Clin Exp Neuropsychol. 2006;28:1113–26.
Ames GE, Heckman MG, Grothe KB, Clark MM. Eating self-efficacy: development of a short-form WEL. Eat Behav. 2012;13:375–8.
Lamm C, Pine D, Fox N. Impact of negative affectively charged stimuli and response style on cognitive-control-related neural activation: an ERP study. Brain Cogn. 2013;83:234–43.
Vacha-Haase T, Thompson B. How to estimate and interpret various effect sizes. J Couns Psychol. 2004;51:473.
Hoaglin DC, Iglewicz B. Fine-tuning some resistant rules for outlier labeling. J Am Stat Assoc. 1987;82:1147–9.
Chalmers DK, Bowyer CA, Olenick NL. Problem drinking and obesity: a comparison in personality patterns and life-style. Int J Addict. 1990;25:803–17.
Reinert KRS, Po'e EK, Barkin SL. The relationship between executive function and obesity in children and adolescents: a systematic literature review. J Obes. 2013;2013:10.
Nederkoorn C, Braet C, Van Eijs Y, Tanghe A, Jansen A. Why obese children cannot resist food: the role of impulsivity. Eat Behav. 2006;7:315–22.
Tottenham N, Hare TA, Casey B. Behavioral assessment of emotion discrimination, emotion regulation, and cognitive control in childhood, adolescence, and adulthood. Front Psychol. 2011;2:39.
Donkers FC, Van Boxtel GJ. The N2 in go/no-go tasks reflects conflict monitoring not response inhibition. Brain Cogn. 2004;56:165–76.
Enriquez-Geppert S, Konrad C, Pantev C, Huster RJ. Conflict and inhibition differentially affect the N200/P300 complex in a combined go/nogo and stop-signal task. NeuroImage. 2010;51:877–87.
Smith JL, Johnstone SJ, Barry RJ. Movement-related potentials in the Go/NoGo task: the P3 reflects both cognitive and motor inhibition. Clin Neurophysiol. 2008;119:704–14.
Acknowledgments
We wish to thank all the research assistants at the Neurobiological Lab for Learning and Development (NLD) who have helped with the data collection. This work was supported by the Transforming Lives grant (Woltering) awarded in 2015 by the College of Education and Human Development at Texas A&M University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
The present study was approved by the Institutional Research Ethic Board (IRB) at Texas A&M University (protocol reference: IRB2010-0877D). All participants and one of their guardians provided informed written consent prior to the start of the study
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Chen, S., Jia, Y. & Woltering, S. Neural differences of inhibitory control between adolescents with obesity and their peers. Int J Obes 42, 1753–1761 (2018). https://doi.org/10.1038/s41366-018-0142-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41366-018-0142-x
This article is cited by
-
Exploring the effects of habituation and scent in first-person 360-degree videos on consumption behavior
Scientific Reports (2023)
-
Weight spectrum and executive function in adolescents: the moderating role of negative emotions
Child and Adolescent Psychiatry and Mental Health (2022)
-
Diminished Inhibitory Control in Adolescents with Overweight and/or Substance Use: an ERP Study
International Journal of Mental Health and Addiction (2022)
-
Neural Correlates of Attentional Bias to Food Stimuli in Obese Adolescents
Brain Topography (2021)
-
Attentional bias and response inhibition in severe obesity with food disinhibition: a study of P300 and N200 event-related potential
International Journal of Obesity (2020)