Maternal Error-Related Negativity Relations with Offspring Error-Related Negativity and Negative Parenting Styles: A Novel Model of Internalizing Psychopathology Risk

  • Author Footnotes
    1 Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA.
    Jennifer H. Suor
    Correspondence
    Address correspondence concerning this article to Jennifer H. Suor, Department of Psychiatry, University of Illinois at Chicago, 1601 W. Taylor Street, Chicago, IL, 60608, USA; Phone: (312) 355- 3871.
    Footnotes
    1 Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA.
    Search for articles by this author
  • Author Footnotes
    1 Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA.
    Alison E. Calentino
    Footnotes
    1 Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA.
    Search for articles by this author
  • Author Footnotes
    1 Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA.
    ,
    Author Footnotes
    2 Department of Psychology, University of Illinois at Chicago, Chicago, IL, USA.
    Maria Granros
    Footnotes
    1 Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA.
    2 Department of Psychology, University of Illinois at Chicago, Chicago, IL, USA.
    Search for articles by this author
  • Katie L. Burkhouse
    Search for articles by this author
  • Author Footnotes
    1 Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA.
    2 Department of Psychology, University of Illinois at Chicago, Chicago, IL, USA.
Published:October 21, 2021DOI:https://doi.org/10.1016/j.bpsc.2021.10.007

      Abstract

      Background

      Enhanced error-related negativity (ERN), an event-related potential (ERP) component reflecting neural sensitivity to errors and threat, has been theorized to represent an endophenotype of internalizing psychopathologies (IPs). We tested whether intergenerational transmission of ERN patterns may confer risk for internalizing symptoms. We examined associations among maternal and offspring ERN, and offspring internalizing symptoms. Given the role of parenting in IP risk, we also explored how maternal negative parenting styles related to maternal ERN and offspring internalizing symptoms.

      Methods

      Participants included 117 biological mother-child dyads (ages 9-16 years, 70.9% female). Seventy-two mothers had a history of major depression (32 with lifetime anxiety) and 45 had no history of psychiatric illness. Dyads completed psychiatric interviews, parenting questionnaires, and a flanker task to elicit the ERN while electroencephalogram (EEG) was recorded.

      Results

      Path analyses revealed that maternal ERN was significantly associated with enhanced offspring ERN and greater negative parenting styles. Enhanced offspring ERN and maternal negative parenting styles were significantly related to greater internalizing symptoms in offspring. Maternal ERN had a significant indirect effect on offspring internalizing symptoms through offspring ERN and maternal negative parenting styles, above the effects of self-reported maternal internalizing symptoms. Maternal IP history did not moderate pathways.

      Conclusions

      Study findings suggest enhanced maternal ERN is indirectly associated with greater offspring internalizing symptoms through its relations to offspring ERN and negative parenting styles. Future longitudinal work is needed to evaluate the temporal timing and directionality of these tested pathways and their clinical implications for the prevention of IPs.
      The UIC Institutional Review Board approved study procedures prior to data collection. Informed consent and assent was obtained from mothers and their offspring after study procedures were explained to them.

      Keywords

      To read this article in full you will need to make a payment

      References

        • Essau C.A.
        • Lewinsohn P.M.
        • Olaya B.
        • Seeley J.R.
        Anxiety disorders in adolescents and psychosocial outcomes at age 30.
        J Affect Disord. 2014; 163: 125-132
        • Pettit J.W.
        • Lewinsohn P.M.
        • Roberts R.E.
        • Seeley J.R.
        • Monteith L.
        The long-term course of depression: Development of an empirical index and identification of early adult outcomes.
        Psychol Med. 2009; 39: 403-412
        • Garber J.
        • Weersing V.R.
        Comorbidity of anxiety and depression in youth: Implications for treatment and prevention.
        Clin Psychol. 2010; 17: 293-306
        • Cosgrove V.E.
        • Rhee S.H.
        • Gelhorn H.L.
        • Boeldt D.
        • Corley R.C.
        • Ehringer M.A.
        • et al.
        Structure and etiology of co-occurring internalizing and externalizing disorders in adolescents.
        J Abnorm Child Psychol. 2011; 39: 109-123
        • Hettema J.M.
        • Bourdon J.L.
        • Sawyers C.
        • Verhulst B.
        • Brotman M.A.
        • Leibenluft E.
        • et al.
        Genetic and environmental risk structure of internalizing psychopathology in youth.
        Depress Anxiety. 2020; 37: 540-548
        • Lebowitz E.R.
        • Leckman J.F.
        • Silverman W.K.
        • Feldman R.
        Cross-generational influences on childhood anxiety disorders: Pathways and mechanisms.
        J Neural Transm. 2016; 123: 1053-1067
        • Ghandour R.M.
        • Sherman L.J.
        • Vladutiu C.J.
        • Ali M.M.
        • Lynch S.E.
        • Bitsko R.H.
        • Blumberg S.J.
        Prevalence and treatment of depression, anxiety, and conduct problems in us children.
        J Pediatr. 2019; 206: 256-267
        • Falkenstein M.
        • Hohnsbein J.
        • Hoormann J.
        • Blanke L.
        Effects of crossmodal divided attention on late ERP components. II. Error processing in choice reaction tasks.
        Electroencephalogr Clin Neurophysiol. 1991; 78: 447-455
        • Gehring W.J.
        • Goss B.
        • Coles M.G.H.
        • Meyer D.E.
        • Donchin E.
        A neural system for error detection and compensation.
        Psychol Sci. 1993; 4: 385-390
        • Debener S.
        • Ullsperger M.
        • Siegel M.
        • Fiehler K.
        • Von Cramon D.Y.
        • Engel A.K.
        Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring.
        J Neurosci. 2005; 25: 11730-11737
        • Dehaene S.
        • Posner M.I.
        • Tucker D.M.
        Localization of a neural system for error detection and compensation.
        Psychol Sci. 1994; 5: 303-305
        • Riesel A.
        • Endrass T.
        • Kaufmann C.
        • Kathmann N.
        Overactive error-related brain activity as a candidate endophenotype for obsessive-compulsive disorder: Evidence from unaffected first-degree relatives.
        Am J Psychiatry. 2011; 168: 317-324
        • Yeung N.
        • Botvinick M.M.
        • Cohen J.D.
        The neural basis of error detection: Conflict monitoring and the error-related negativity.
        Psychol Rev. 2004; 111: 931-959
        • Weinberg A.
        • Riesel A.
        • Hajcak G.
        Integrating multiple perspectives on error-related brain activity: The ERN as a neural indicator of trait defensive reactivity.
        Motiv Emot. 2012; 36: 84-100
        • Foti D.
        • Kotov R.
        • Hajcak G.
        Psychometric considerations in using error-related brain activity as a biomarker in psychotic disorders.
        J Abnorm Psychol. 2013; 122: 520-531
        • Olvet D.M.
        • Hajcak G.
        Reliability of error-related brain activity.
        Brain Res. 2009; 1284: 89-99
        • Meyer A.
        A biomarker of anxiety in children and adolescents: A review focusing on the error-related negativity (ERN) and anxiety across development.
        Dev Cogn Neurosci. 2017; 27: 58-68
        • Meyer A.
        • Hajcak G.
        • Torpey-Newman D.C.
        • Kujawa A.
        • Klein D.N.
        Enhanced error-related brain activity in children predicts the onset of anxiety disorders between the ages of 6 and 9.
        J Abnorm Psychol. 2015; 124: 266-274
        • Meyer A.
        • Nelson B.
        • Perlman G.
        • Klein D.N.
        • Kotov R.
        A neural biomarker, the error-related negativity, predicts the first onset of generalized anxiety disorder in a large sample of adolescent females.
        J Child Psychol Psychiatry. 2018; 59: 1162-1170
        • Aarts K.
        • Vanderhasselt M.-A.
        • Otte G.
        • Baeken C.
        • Pourtois G.
        Electrical brain imaging reveals the expression and timing of altered error monitoring functions in major depression.
        J Abnorm Psychol. 2013; 122: 939-950
        • Chiu P.H.
        • Deldin P.J.
        Neural evidence for enhanced error detection in major depressive disorder.
        AJP. 2007; 164: 608-616
        • Ruchsow M.
        • Herrnberger B.
        • Beschoner P.
        • Grön G.
        • Spitzer M.
        • Kiefer M.
        Error processing in major depressive disorder: Evidence from event-related potentials.
        J Psychiatr Res. 2006; 40: 37-46
        • Ruchsow M.
        • Herrnberger B.
        • Wiesend C.
        • Grön G.
        • Spitzer M.
        • Kiefer M.
        The effect of erroneous responses on response monitoring in patients with major depressive disorder: A study with event-related potentials.
        Psychophysiology. 2004; 41: 833-840
        • Weinberg A.
        • Kotov R.
        • Proudfit G.H.
        Neural indicators of error processing in generalized anxiety disorder, obsessive-compulsive disorder, and major depressive disorder.
        J Abnorm Psychol. 2015; 124: 172-185
        • Olvet D.M.
        • Klein D.N.
        • Hajcak G.
        Depression symptom severity and error-related brain activity.
        Psychiatry Res. 2010; 179: 30-37
        • Hajcak G.
        • McDonald N.
        • Simons R.F.
        Error-related psychophysiology and negative affect.
        Brain Cogn. 2004; 56: 189-197
        • Olvet D.M.
        • Hajcak G.
        The error-related negativity (ERN) and psychopathology: Toward an endophenotype.
        Clin Psychol Rev. 2008; 28: 1343-1354
        • Anokhin A.P.
        • Golosheykin S.
        • Heath A.C.
        Heritability of frontal brain function related to action monitoring.
        Psychophysiology. 2008; 45: 524-534
        • Burwell S.J.
        • Malone S.M.
        • Iacono W.G.
        One-year developmental stability and covariance among oddball, novelty, go/no-go, and flanker event-related potentials in adolescence: A monozygotic twin study.
        Psychophysiology. 2016; 53: 991-1007
        • Moser J.S.
        • Fisher M.
        • Hicks B.M.
        • Zucker R.A.
        • Durbin C.E.
        Feedback-related neurophysiology in children and their parents: Developmental differences, familial transmission, and relationship to error-monitoring.
        Int J Psychophysiol. 2018; 132: 338-352
        • Riesel A.
        • Klawohn J.
        • Grützmann R.
        • Kaufmann C.
        • Heinzel S.
        • Bey K.
        • et al.
        Error-related brain activity as a transdiagnostic endophenotype for obsessive-compulsive disorder, anxiety and substance use disorder.
        Psychol Med. 2019; 49: 1207-1217
        • Burkhouse K.L.
        • Uhrlass D.J.
        • Stone L.B.
        • Knopik V.S.
        • Gibb B.E.
        Expressed emotion-criticism and risk of depression onset in children.
        J Clin Child Adolesc Psychol. 2012; 41: 771-777
        • Goodman S.H.
        • Simon H.F.M.
        • Shamblaw A.L.
        • Kim C.Y.
        Parenting as a mediator of associations between depression in mothers and children’s functioning: A systematic review and meta-analysis.
        Clin Child Fam Psychol Rev. 2020; 23: 427-460
        • Brooker R.J.
        • Buss K.A.
        Harsh parenting and fearfulness in toddlerhood interact to predict amplitudes of preschool error-related negativity.
        Dev Cogn Neurosci. 2014; 9: 148-159
        • Meyer A.
        • Proudfit G.H.
        • Bufferd S.J.
        • Kujawa A.J.
        • Laptook R.S.
        • Torpey D.C.
        • Klein D.N.
        Self-reported and observed punitive parenting prospectively predicts increased error-related brain activity in six-year-old children.
        J Abnorm Child Psychol. 2015; 43: 821-829
        • Meyer A.
        • Wissemann K.
        Controlling parenting and perfectionism is associated with an increased error-related negativity (ERN) in young adults.
        Soc Cogn Affect Neurosci. 2020; 15: 87-95
        • Banica I.
        • Sandre A.
        • Weinberg A.
        Overprotective/authoritarian maternal parenting is associated with an enhanced error-related negativity (ERN) in emerging adult females.
        Int J Psychophysiol. 2019; 137: 12-20
        • Chong L.J.
        • Mirzadegan I.A.
        • Meyer A.
        The association between parenting and the error-related negativity across childhood and adolescence.
        Dev Cogn Neurosci. 2020; 45: 100852
        • Meyer A.
        • Carlton C.
        • Chong L.J.
        • Wissemann K.
        The presence of a controlling parent is related to an increase in the error-related negativity in 5–7 year-old children.
        J Abnorm Child Psychol. 2019; 47: 935-945
        • Goodman S.H.
        Intergenerational transmission of depression.
        Annu Rev Clin Psychol. 2020; 16: 213-238
        • Barrett J.
        • Fleming A.S.
        Annual Research Review: All mothers are not created equal: Neural and psychobiological perspectives on mothering and the importance of individual differences.
        J Child Psychol Psychiatry. 2011; 52: 368-397
      1. First MB, Williams JBW, Karg RS, Spitzer RL (2015): Structured Clinical Interview for DSM-5—Research Version (SCID-5 for DSM-5, Research Version; SCID-5-RV). Arlington, VA: American Psychiatric Association.

      2. Kaufman J, Birmaher B, Axelson D, Perepletchikova F, Brent D, Ryan N (2016): The KSADS-PL DSM-5. Baltimore, MD: Kennedy Krieger Institute.

      3. Achenbach T M, Rescorla L A (2001): Manual for the ASEBA School-Age Forms & Profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, & Families.

        • Beck A.T.
        • Epstein N.
        • Brown G.
        • Steer R.A.
        An inventory for measuring clinical anxiety: Psychometric properties.
        J Consult Clin Psychol. 1988; 56: 893-897
        • Beck A.T.
        • Steer R.A.
        • Brown G.
        Beck Depression Inventory–II.
        Psychol Assess. 1996; 67: 588-597
        • Hooley J.M.
        • Teasdale J.D.
        Predictors of relapse in unipolar depressives: Expressed emotion, marital distress, and perceived criticism.
        J Abnorm Psychol. 1989; 98: 229-235
        • Parker G.
        • Tupling H.
        • Brown L.B.
        A parental bonding instrument.
        Br J Med Psychol. 1979; 52: 1-10
        • Little R.J.A.
        A test of missing completely at random for multivariate data with missing values.
        J Am Stat Assoc. 1988; 83: 1198-1202
        • Schlomer G.L.
        • Bauman S.
        • Card N.A.
        Best practices for missing data management in counseling psychology.
        J Couns Psychol. 2010; 57: 1-10
        • Enders C.K.
        The impact of nonnormality on full information maximum-likelihood estimation for structural equation models with missing data.
        Psychol Methods. 2001; 6: 352-370
        • Hu L.
        • Bentler P.M.
        Cutoff criteria for fit indexes in covariance structure analysis: Conventional criteria versus new alternatives.
        Struct Equ Model. 1999; 6: 1-55
        • Bentler P.M.
        Comparative fit indexes in structural models.
        Psychol Bull. 1990; 107: 238-246
      4. Steiger JH, Lind J (1980): Statistically based tests for the number of common factors. Paper presented at the annual meeting of the Psychometric Society, IA.

        • Hayes A.F.
        Beyond Baron and Kenny: Statistical Mediation Analysis in the New Millennium.
        Commun Monogr. 2009; 76: 408-420
        • MacKinnon D.P.
        • Krull J.L.
        • Lockwood C.M.
        Equivalence of the mediation, confounding and suppression effect.
        Prev Sci. 2000; 1: 173-181
        • MacKinnon D.P.
        • Fritz M.S.
        • Williams J.
        • Lockwood C.M.
        Distribution of the product confidence limits for the indirect effect: Program PRODCLIN.
        Behav Res Methods. 2007; 39: 384-389
        • Tofighi D.
        • MacKinnon D.P.
        RMediation: An R package for mediation analysis confidence intervals.
        Behav Res. 2011; 43: 692-700
      5. Rothbart M K, Derryberry D, Posner M I (1994): A psychobiological approach to the development of temperament. In: Bates JE, Wachs TD,editors. Temperament: Individual Differences at the Interface of Biology and Behavior. Washington, DC: American Psychological Association, pp 83-116.

        • Wachs T.D.
        • Pollitt E.
        • Cueto S.
        • Jacoby E.
        Structure and cross-contextual stability of neonatal temperament.
        Infant Behav Dev. 2004; 27: 382-396
        • Goodman S.H.
        • Rouse M.H.
        • Connell A.M.
        • Broth M.R.
        • Hall C.M.
        • Heyward D.
        Maternal depression and child psychopathology: A meta-analytic review.
        Clin Child Fam Psychol Rev. 2011; 14: 1-27
        • Lovejoy M.C.
        • Graczyk P.A.
        • O'Hare E.
        • Neuman G.
        Maternal depression and parenting behavior: A meta-analytic review.
        Clin Psychol Rev. 2000; 20: 561-592
        • Breslend N.L.
        • Parent J.
        • Forehand R.
        • Peisch V.
        • Compas B.E.
        Children of parents with a history of depression: The impact of a preventive intervention on youth social problems through reductions in internalizing problems.
        Dev Psychopathol. 2019; 31: 219-231
        • Chahal R.
        • Kirshenbaum J.S.
        • Ho T.C.
        • Mastrovito D.
        • Gotlib I.H.
        Greater age-related changes in white matter morphometry following early life stress: Associations with internalizing problems in adolescence.
        Dev Cogn Neurosci. 2021; 47: 100899
        • Ebesutani C.
        • Bernstein A.
        • Martinez J.I.
        • Chorpita B.F.
        • Weisz J.R.
        The youth self report: Applicability and validity across younger and older youths.
        J Clin Child Adolesc Psychol. 2011; 40: 338-346
        • Klawohn J.
        • Hajcak G.
        • Amir N.
        • Kathmann N.
        • Riesel A.
        Application of attentional bias modification training to modulate hyperactive error-monitoring in OCD.
        Int J Psychophysiol. 2020; 156: 79-86
        • Meyer A.
        • Gibby B.
        • Wissemann K.
        • Klawohn J.
        • Hajcak G.
        • Schmidt N.B.
        A brief, computerized intervention targeting error sensitivity reduces the error-related negativity.
        Cogn Affect Behav Neurosci. 2020; 20: 172-180