Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Pediatrics

Retrieval-induced forgetting in children and adolescents with and without obesity

International Journal of Obesity volume 46, pages 851–858 (2022)Cite this article

Subjects

Abstract

Background/objectives

Previous research indicates that youth with obesity exhibit deficits in executive functioning (EF), which often take the form of impaired response inhibition. One aspect of EF not previously studied in obesity is the adaptive process known as retrieval-induced forgetting (RIF), the suppression/inhibition of intrusive or non-target items by the retrieval of specific items from memory. The present study investigated if child or adolescent obesity disrupts the ability to inhibit retrieval of intrusive memories.

Subjects/methods

We compared the manifestation of RIF in children (ages 8–12) and adolescents (ages 13–18) as a function of their weight status and sex. We also evaluated the effects of these variables on simple recall of items from episodic memory under conditions where competition from intrusive items was reduced.

Results

Children with obesity did not demonstrate significant RIF, whereas RIF was exhibited by preteens without obesity and by teenage participants with- and without obesity (Weight Status × Age Group interaction p = 0.028). This pattern of results did not differ as a function of sex for either age group. No differences in episodic memory were found. Additional analyses using Age as continuous covariate (and not as a nominal group) comparing participants who exhibited RIF with those who did not, found that the no RIF group consumed fast-food meals more frequently (p = 0.024) and had higher percentages of total body adiposity and android fat compared to the RIF group (p’s < 0.05).

Conclusions

The findings expand what is known about the effects of childhood obesity on cognitive functioning, identify impaired RIF with specific behavioral and dietary factors and increased adiposity, and suggest the possibility that impairments in the ability to inhibit intrusive memories of food and eating may contribute to poor early-life weight control.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Proportion of RP + items recalled by preteens and teens with and without obesity.
Fig. 2: Proportion of RP- and NRP- items recalled by preteens and teens with and without obesity.
Fig. 3: Proportion of RP- and NRP- items recalled by preteens and teens with high and low adiposity.

Similar content being viewed by others

References

  1. Ogden CL, Fryar CD, Martin CB, Freedman DS, Carroll MD, Gu Q, et al. Trends in Obesity Prevalence by Race and Hispanic Origin-1999-2000 to 2017-2018. JAMA. 2020;324:1208–10.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Fields LC, Brown C, Skelton JA, Cain KS, Cohen GM. Internalized Weight Bias, Teasing, and Self-Esteem in Children with Overweight or Obesity. Child Obes. 2021;17:43–50.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kumar S, Kelly AS. Review of childhood obesity: from epidemiology, etiology, and comorbidities to clinical assessment and treatment. Mayo Clin Proc. 2017;92:251–65.

    Article  PubMed  Google Scholar 

  4. Rankin J, Matthews L, Cobley S, Han A, Sanders R, Wiltshire HD, et al. Psychological consequences of childhood obesity: psychiatric comorbidity and prevention. Adolesc Health Med Ther. 2016;7:125–46.

    PubMed  PubMed Central  Google Scholar 

  5. Diamond A. Executive functions. Annu Rev Psychol. 2013;64:135–68.

    Article  PubMed  Google Scholar 

  6. Yang Y, Shields GS, Guo C, Liu Y. Executive function performance in obesity and overweight individuals: a meta-analysis and review. Neurosci Biobehav Rev. 2018;84:225–44.

    Article  PubMed  Google Scholar 

  7. Mamrot P, Hanc T. The association of the executive functions with overweight and obesity indicators in children and adolescents: a literature review. Neurosci Biobehav Rev. 2019;107:59–68.

    Article  PubMed  Google Scholar 

  8. Liang J, Matheson BE, Kaye WH, Boutelle KN. Neurocognitive correlates of obesity and obesity-related behaviors in children and adolescents. Int J Obesity. 2005;2014:494–506.

    Google Scholar 

  9. Friedman NP, Miyake A. Unity and diversity of executive functions: Individual differences as a window on cognitive structure. Cortex. 2017;86:186–204.

    Article  PubMed  Google Scholar 

  10. Martin AA, Davidson TL. Childhood Obesity: Implications for Neurocognitive Functioning. In: Goran MI, (ed). Childhood Obesity: Causes, Consequences, and Intervention Approaches. Boca Raton, CRC Press; 2017. p. 255–71.

  11. Sprondel V, Kipp KH, Mecklinger A. Developmental Changes in Item and Source Memory: Evidence From an ERP Recognition Memory Study With Children, Adolescents, and Adults. Child Dev. 2011;82:1638–953.

    Article  PubMed  Google Scholar 

  12. Lechuga MT, Moreno V, Pelegrina S, Gómez-Ariza CJ, Bajo MT. Age differences in memory control: Evidence from updating and retrieval-practice tasks. Acta Psychologica. 2006;123:279–98.

    Article  PubMed  Google Scholar 

  13. Pelegrina S, Molina R, Rodríguez-Martínez EI, Linares R, Gómez CM. Age-related changes in selection, recognition, updating and maintenance information in WM. An ERP study in children and adolescents. Biol Psychol. 2020;157. https://doi.org/10.1016/j.biopsycho.2020.107977.

  14. Hartung J, Engelhardt LE, Thibodeaux ML, Harden KP, Tucker-Drob EM. Developmental transformations in the structure of executive functions. J Exp Child Psychol. 2020;189. https://doi.org/10.1016/j.jecp.2019.104681.

  15. Zanini GAV, Miranda MC, Cogo-Moreira H, Nouri A, Fernández AL, Pompéia S. An Adaptable, Open-Access Test Battery to Study the Fractionation of Executive-Functions in Diverse Populations. Front Psychol. 2021;12:627219.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Storm BC, Levy BJ. A progress report on the inhibitory account of retrieval-induced forgetting. Mem Cognit. 2012;40:827–43.

    Article  PubMed  Google Scholar 

  17. Ford RM, Keating S, Patel R. Retrieval-induced forgetting: a developmental study. British J Dev Psychol. 2004;22:585–603.

    Article  Google Scholar 

  18. Zellner M, Bauml KH. Intact retrieval inhibition in children’s episodic recall. Mem Cognit. 2005;33:396–404.

    Article  PubMed  Google Scholar 

  19. Kuczmarski RJ, Ogden CL, Grummer-Strawn LM, Flegal KM, Guo SS, Wei R, et al. CDC growth charts: United States. Adv Data 2000:1–27.

  20. Wechsler D, Pearson. Wechsler Abbreviated Scale of Intelligence. 2nd ed. Bloomington, MN, Pearson; 2011.

  21. Byrne ME, Shank LM, Altman DR, Swanson TN, Ramirez E, Moore NA, et al. Inhibitory control and negative affect in relation to food intake among youth. Appetite. 2021;156:104858.

    Article  PubMed  Google Scholar 

  22. Byrne ME, Shomaker LB, Brady SM, Kozlosky M, Yanovski JA, Tanofsky-Kraff M. Associations between latent trait negative affect and patterns of food-intake among girls with loss-of-control eating. Int J Eat Disord. 2020;53:618–24.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Byrne ME, Tanofsky-Kraff M, Jaramillo M, Shank LM, LeMay-Russell S, Rubin SG et al. Relationships of Trait Anxiety and Loss of Control Eating with Serum Leptin Concentrations among Youth. Nutrients. 2019;11. https://doi.org/10.3390/nu11092198.

  24. Kelly NR, Jaramillo M, Ramirez S, Altman DR, Rubin SG, Yang SB, et al. Executive functioning and disinhibited eating in children and adolescents. Pediatr Obes. 2020;15:e12614.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Mi SJ, Kelly NR, Brychta RJ, Grammer AC, Jaramillo M, Chen KY, et al. Associations of sleep patterns with metabolic syndrome indices, body composition, and energy intake in children and adolescents. Pediatr Obes. 2019;14:e12507.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Shank LM, Tanofsky-Kraff M, Kelly NR, Jaramillo M, Rubin SG, Altman DR, et al. The association between alexithymia and eating behavior in children and adolescents. Appetite. 2019;142:104381.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, et al. 2000 CDC Growth Charts for the United States: methods and development. Vital Health Stat. 2002;11:1–190.

    Google Scholar 

  28. Samsell L, Regier M, Walton C, Cottrell L. Importance of Android/Gynoid Fat Ratio in Predicting Metabolic and Cardiovascular Disease Risk in Normal Weight as well as Overweight and Obese Children. J Obesity. 2014;2014. https://doi.org/10.1155/2014/846578.

  29. Dordevic AL, Bonham M, Ghasem-Zadeh A, Evans A, Barber E, Day K, et al. Reliability of compartmental body composition measures in weight-stable adults using ge iDXA: implications for research and practice. Nutrients. 2018;10. https://doi.org/10.3390/nu10101484.

  30. NHANES. No Title. Epidemiology and Genomics Research Program, Dietary Screener Questionnaires (DSQ) in the NHANES 2009-10: DSQ. 2009. https://epi.grants.cancer.gov/nhanes/dietscreen/questionnaires.html.

  31. Tanofsky-Kraff M, McDuffie JR, Yanovski SZ, Kozlosky M, Schvey NA, Shomaker LB, et al. Laboratory assessment of the food intake of children and adolescents with loss of control eating. Am J Clin Nutr. 2009;89:738–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Anderson MC, Bjork RA, Bjork EL. Remembering can cause forgetting: retrieval dynamics in long-term memory. J Exp Psychol Learn Mem Cogn. 1994;20:1063–87.

    Article  CAS  PubMed  Google Scholar 

  33. Flegal KM, Ogden CL, Yanovski JA, Freedman DS, Shepherd JA, Graubard BI, et al. High adiposity and high body mass index-for-age in US children and adolescents overall and by race-ethnic group. Am J Clin Nutr. 2010;91:1020–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Borrud LG, Flegal KM, Looker AC, Everhart JE, Harris TB, Shepherd JA. Body Composition Data for Individuals 8 Years of Age and Older: U.S. Population, 1999–2004. Vital Health Statistics Series 11, Data Natl Health Survey. 2010;11:1.

    Google Scholar 

  35. George D, Mallery M. Communication, procedural justice and employee attitude: relation under condition of divestiture. In: SPSS for Windows step by step: A simple guide and reference 17.0 update (10th ed.). Boston, MA, Pearson; 2010. p. 63–83.

  36. Hair JF, Black WC, Babin BJ, Anderson RE. Multivariate data analysis. 7th ed. Englewood Cliffs, NJ, Prentice-Hall; 2010.

  37. Abdul Rahman A, Carroll DJ, Espy KA, Wiebe SA. Neural Correlates of Response Inhibition in Early Childhood: Evidence From a Go/No-Go Task. Dev Neuropsychol. 2017;42:336–50.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Tillman CM, Thorell LB, Brocki KC, Bohlin G. Motor response inhibition and execution in the stop-signal task: development and relation to ADHD behaviors. Child Neuropsychol. 2008;14:42–59.

    Article  PubMed  Google Scholar 

  39. Braet C, Crombez G. Cognitive interference due to food cues in childhood obesity. J Clin Child Adolesc Psychol. 2003;32:32–9.

    Article  PubMed  Google Scholar 

  40. Fogel A, McCrickerd K, Goh AT, Fries LR, Chong YS, Tan KH, et al. Associations between inhibitory control, eating behaviours and adiposity in 6-year-old children. Int J Obes (Lond). 2019;43:1344–53.

    Article  Google Scholar 

  41. Gerdan G, Kurt M. Response inhibition according to the stimulus and food type in exogenous obesity. Appetite. 2020;150:104651.

    Article  PubMed  Google Scholar 

  42. Nijs IM, Franken IH, Muris P. Food-related Stroop interference in obese and normal-weight individuals: behavioral and electrophysiological indices. Eat Behav. 2010;11:258–65.

    Article  PubMed  Google Scholar 

  43. Rebello CJ, Greenway FL. Reward-Induced Eating: Therapeutic Approaches to Addressing Food Cravings. Adv Ther. 2016;33:1853–66.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Rogers PJ. Food and drug addictions: similarities and differences. Pharmacol Biochem Behav. 2017;153:182–90.

    Article  CAS  PubMed  Google Scholar 

  45. Sun W, Kober H. Regulating food craving: From mechanisms to interventions. Physiol Behav. 2020;222:112878.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Lynch KM, Page KA, Shi Y, Xiang AH, Toga AW, Clark KA. The effect of body mass index on hippocampal morphology and memory performance in late childhood and adolescence. Hippocampus. 2021;31:189–200.

    Article  PubMed  Google Scholar 

  47. Wimber M, Bäuml KH, Bergström Z, Markopoulos G, Heinze HJ, Richardson-Klavehn A. Neural markers of inhibition in human memory retrieval. J Neurosci. 2008;28:13419–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Wimber M, Rutschmann RM, Greenlee MW, Bäuml KH. Retrieval from episodic memory: neural mechanisms of interference resolution. J Cogn Neurosci. 2009;21:538–49.

    Article  PubMed  Google Scholar 

  49. Koolschijn RS, Emir UE, Pantelides AC, Nili H, Behrens TEJ, Barron HC. The Hippocampus and Neocortical Inhibitory Engrams Protect against Memory Interference. Neuron. 2019;101:528–.e6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Schmitz TW, Correia MM, Ferreira CS, Prescot AP, Anderson MC. Hippocampal GABA enables inhibitory control over unwanted thoughts. Nat Commun. 2017;8:1311.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Pearce AL, Mackey E, Cherry JBC, Olson A, You X, Nadler EP, et al. Altered neural correlates of episodic memory in adolescents with severe obesity. Dev Cogn Neurosci. 2019;40:100727.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Khan NA, Baym CL, Monti JM, Raine LB, Drollette ES, Scudder MR, et al. Central Adiposity Is Negatively Associated with Hippocampal-Dependent Relational Memory among Overweight and Obese Children. J Pediatrics. 2015;166:302–308.e1.

    Article  Google Scholar 

  53. Steinberger J, Jacobs DR, Raatz S, Moran A, Hong CP, Sinaiko AR. Comparison of body fatness measurements by BMI and skinfolds vs dual energy X-ray absorptiometry and their relation to cardiovascular risk factors in adolescents. Int J Obesity. 2005;29:1346–52.

    Article  CAS  Google Scholar 

  54. Hudda MT, Aarestrup J, Owen CG, Cook DG, Sørensen TIA, Rudnicka AR, et al. Association of Childhood Fat Mass and Weight with Adult-Onset Type 2 Diabetes in Denmark. JAMA Network Open 2021;4. https://doi.org/10.1001/jamanetworkopen.2021.8524.

  55. Jia P, Luo M, Li Y, Zheng JS, Xiao Q, Luo J. Fast-food restaurant, unhealthy eating, and childhood obesity: A systematic review and meta-analysis. Obes Rev. 2021;22:e12944.

    PubMed  Google Scholar 

  56. Poorolajal J, Sahraei F, Mohamdadi Y, Doosti-Irani A, Moradi L. Behavioral factors influencing childhood obesity: a systematic review and meta-analysis. Obes Res Clin Pract. 2020;14:109–18.

    Article  PubMed  Google Scholar 

  57. Attuquayefio T, Stevenson RJ, Boakes RA, Oaten MJ, Yeomans MR, Mahmut M, et al. A high-fat high-sugar diet predicts poorer hippocampal-related memory and a reduced ability to suppress wanting under satiety. J Exp Psychol Anim Learn Cogn. 2016;42:415–28.

    Article  PubMed  Google Scholar 

  58. Hsu TM, Konanur VR, Taing L, Usui R, Kayser BD, Goran MI, et al. Effects of sucrose and high fructose corn syrup consumption on spatial memory function and hippocampal neuroinflammation in adolescent rats. Hippocampus. 2015;25:227–39.

    Article  CAS  PubMed  Google Scholar 

  59. Khan NA, Raine LB, Drollette ES, Scudder MR, Hillman CH. The relation of saturated fats and dietary cholesterol to childhood cognitive flexibility. Appetite. 2015. https://doi.org/10.1016/j.appet.2015.04.012.

  60. Liu Q, Guo J, Hu L, Veronese N, Smith L, Yang L, et al. Association between Intake of Energy and Macronutrients and Memory Impairment Severity in US Older Adults, National Health and Nutrition Examination Survey 2011-2014. Nutrients. 2020;12. https://doi.org/10.3390/nu12113559.

  61. Tsan L, Décarie-Spain L, Noble EE, Kanoski SE. Western Diet Consumption During Development: Setting the Stage for Neurocognitive Dysfunction. Front Neurosci. 2021;15:632312.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Hargrave SL, Jones S, Davidson TL. The Outward Spiral: a vicious cycle model of obesity and cognitive dysfunction. Curr Opin Behav Sci. 2016;9:40–46.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Davidson TL, Jones S, Roy M, Stevenson RJ. The Cognitive Control of Eating and Body Weight: It’s More Than What You “Think. Front Psychol. 2019;10:62.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Hoyland A, Dye L, Lawton CL. A systematic review of the effect of breakfast on the cognitive performance of children and adolescents. Nutr Res Rev. 2009;22:220–43.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the participants and their parents for their involvement in this trial.

Author information

Authors and Affiliations

  1. Department of Neuroscience, American University, 4400 Massachusetts Avenue, NW, Washington, DC, 20016, USA

    Terry L. Davidson & Alexia Hyde

  2. Center for Neuroscience and Behavior, American University, 4400 Massachusetts Avenue, NW, Washington, DC, 20016, USA

    Terry L. Davidson, Anastasia Snelling & Sarah Irvine Belson

  3. Section on Growth and Obesity, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), 10 Center Drive, Bethesda, MD, 20892, USA

    Eliana Ramirez, Esther A. Kwarteng, Kweku G. Djan, Loie M. Faulkner, Megan N. Parker, Anna Zenno, Lisa M. Shank, Marian Tanofsky-Kraff & Jack A. Yanovski

  4. Department of Medical and Clinical Psychology, Uniformed Services University of the Health Sciences (USU), 4301 Jones Bridge Road, Bethesda, MD, 20814, USA

    Megan N. Parker, Lisa M. Shank & Marian Tanofsky-Kraff

  5. Nutrition Department, Clinical Research Center, NIH, 10 Center Drive, Bethesda, MD, 20892, USA

    Shanna B. Yang

  6. Department of Counseling Psychology and Human Services, Prevention Science Institute, University of Oregon, Eugene, OR, 97403-5207, USA

    Nichole R. Kelly

  7. Department of Medicine, Military Cardiovascular Outcomes Research (MiCOR), USU, 4301 Jones Bridge Road, Bethesda, MD, 20814, USA

    Lisa M. Shank & Marian Tanofsky-Kraff

  8. Metis Foundation, 300 Convent St #1330, San Antonio, TX, 78205, USA

    Lisa M. Shank

  9. Department of Health Studies, American University, 4400 Massachusetts Avenue, NW, Washington, DC, 20016, USA

    Anastasia Snelling

  10. School of Education, American University, 4400 Massachusetts Avenue, NW, Washington, DC, 20016, USA

    Sarah Irvine Belson

  11. Energy Metabolism Section, Diabetes, Endocrinology, and Obesity Branch, National Institute of Digestive Diseases, Diabetes, and Kidney Disorders, National Institutes of Health (NIH), Department of Health and Human Services (DHHS), 10 Center Drive, Bethesda, MD, 20892, USA

    Kong Y. Chen

Authors
  1. Terry L. Davidson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eliana Ramirez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Esther A. Kwarteng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kweku G. Djan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Loie M. Faulkner
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Megan N. Parker
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shanna B. Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Anna Zenno
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Nichole R. Kelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Lisa M. Shank
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Marian Tanofsky-Kraff
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Anastasia Snelling
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Sarah Irvine Belson
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Alexia Hyde
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Kong Y. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Jack A. Yanovski
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TLD, NRK, MTK, and JAY designed the study; all authors (TLD, ER, EAK, KGD, LMF, MNP, SBY, AZ, NRK, LMS, MTK, AS, SIB, AH, KYC, and JAY) contributed to data collection; TLD conducted data analysis and interpretation, completed the literature search, and with JAY wrote the first draft of the paper and generated the figures. All authors (TLD, ER, EAK, KGD, LMF, MNP, SBY, AZ, NRK, LMS, MTK, AS, SIB, AH, KYC, and JAY) contributed to writing the paper and had final approval of the submitted versions. Dr Sabrina Jones and Dr Lauren McGrath were consulted about data analysis and the distractor task used in the study. This work was supported by Intramural Research Program (NICHD grant number ZIA-HD00641; JAY).

Corresponding author

Correspondence to Terry L. Davidson.

Ethics declarations

Competing interests

The authors report no competing interests for the present work. JAY reports grant support for unrelated projects examining pharmacological treatments of rare syndromes causing obesity from Rhythm Pharmaceuticals Inc. and Soleno Therapeutics, Inc.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Davidson, T.L., Ramirez, E., Kwarteng, E.A. et al. Retrieval-induced forgetting in children and adolescents with and without obesity. Int J Obes 46, 851–858 (2022). https://doi.org/10.1038/s41366-021-01036-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41366-021-01036-5

Search

Advanced search

Quick links