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Persistence, Reward Dependence, and Sensitivity to Reward Are Associated With Unexpected Salience Response in Girls but Not in Adult Women: Implications for Psychiatric Vulnerabilities

Published:April 16, 2021DOI:https://doi.org/10.1016/j.bpsc.2021.04.005

      Abstract

      Background

      Adolescence is a critical period for the development of not only personality but also psychopathology. These processes may be specific to sex, and brain reward circuits may have a role. Here, we studied how reward processing and temperament associations differ across adolescent and adult females.

      Methods

      A total of 29 adolescent girls and 41 adult women completed temperament assessments and performed a classical taste conditioning paradigm during brain imaging. Data were analyzed for the dopamine-related prediction error response. In addition, unexpected stimulus receipt or omission and expected receipt response were also analyzed. Heat maps identified cortical-subcortical brain response associations.

      Results

      Adolescents showed stronger prediction error and unexpected receipt and omission responses (partial η2 = 0.063 to 0.166; p = .001 to .043) in insula, orbitofrontal cortex (OFC), and striatum than adults. Expected stimulus receipt response was similar between groups. In adolescents versus adults, persistence was more strongly positively related to prediction error (OFC, insula, striatum; Fisher’s z = 1.704 to 3.008; p = .001 to .044) and unexpected stimulus receipt (OFC, insula; Fisher’s z = 1.843 to 2.051; p = .014 to .033) and negatively with omission (OFC, insula, striatum; Fisher’s z = −1.905 to −3.069; p = .001 to .028). Reward sensitivity and reward dependence correlated more positively with unexpected stimulus receipt and more negatively with stimulus omission response in adolescents. Adolescents showed significant correlations between the striatum and FC for unexpected stimulus receipt and omission that correlated with persistence but were absent in adults.

      Conclusions

      Associations between temperamental traits and brain reward response may provide neurotypical markers that contribute to developing adaptive or maladaptive behavior patterns when transitioning from adolescence to adulthood.

      Keywords

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      References

        • McAdams D.P.
        • Olson B.D.
        Personality development: Continuity and change over the life course.
        Annu Rev Psychol. 2010; 61: 517-542
        • Rothbart M.K.
        • Ahadi S.A.
        Temperament and the development of personality.
        J Abnorm Psychol. 1994; 103: 55-66
        • Paus T.
        • Keshavan M.
        • Giedd J.N.
        Why do many psychiatric disorders emerge during adolescence?.
        Nat Rev Neurosci. 2008; 9: 947-957
        • Borodinsky L.N.
        • Belgacem Y.H.
        • Swapna I.
        • Sequerra E.B.
        Dynamic regulation of neurotransmitter specification: Relevance to nervous system homeostasis.
        Neuropharmacology. 2014; 78: 75-80
        • Suri D.
        • Teixeira C.M.
        • Cagliostro M.K.
        • Mahadevia D.
        • Ansorge M.S.
        Monoamine-sensitive developmental periods impacting adult emotional and cognitive behaviors.
        Neuropsychopharmacology. 2015; 40: 88-112
        • Kessler R.C.
        • Berglund P.
        • Demler O.
        • Jin R.
        • Merikangas K.R.
        • Walters E.E.
        Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National comorbidity Survey Replication.
        Arch Gen Psychiatry. 2005; 62: 593-602
        • Eaton N.R.
        • Keyes K.M.
        • Krueger R.F.
        • Balsis S.
        • Skodol A.E.
        • Markon K.E.
        • et al.
        An invariant dimensional liability model of gender differences in mental disorder prevalence: Evidence from a national sample.
        J Abnorm Psychol. 2012; 121: 282-288
        • Chaplin T.M.
        • Aldao A.
        Gender differences in emotion expression in children: A meta-analytic review.
        Psychol Bull. 2013; 139: 735-765
        • Dorfman J.
        • Rosen D.
        • Pine D.
        • Ernst M.
        Anxiety and gender influence reward-related processes in children and adolescents.
        J Child Adolesc Psychopharmacol. 2016; 26: 380-390
        • Zahn-Waxler C.
        • Crick N.
        • Shirtcliff E.
        • Woods K.
        The origins and development of psychopathology in females and males.
        in: Cicchetti D. Cohen D. Developmental Psychopathology: Volume 1: Theory and Method. 2nd ed. John Wiley & Sons, Inc., Hoboken, NJ2015: 76-138
        • Ernst M.
        • Pine D.S.
        • Hardin M.
        Triadic model of the neurobiology of motivated behavior in adolescence.
        Psychol Med. 2006; 36: 299-312
        • Cohen J.R.
        • Asarnow R.F.
        • Sabb F.W.
        • Bilder R.M.
        • Bookheimer S.Y.
        • Knowlton B.J.
        • Poldrack R.A.
        A unique adolescent response to reward prediction errors.
        Nat Neurosci. 2010; 13: 669-671
        • O’Doherty J.P.
        • Cockburn J.
        • Pauli W.M.
        Learning, reward, and decision making.
        Annu Rev Psychol. 2017; 68: 73-100
        • Cao Z.
        • Bennett M.
        • Orr C.
        • Icke I.
        • Banaschewski T.
        • Barker G.J.
        • et al.
        Mapping adolescent reward anticipation, receipt, and prediction error during the monetary incentive delay task.
        Hum Brain Mapp. 2019; 40: 262-283
        • Bakker J.M.
        • Goossens L.
        • Kumar P.
        • Lange I.M.J.
        • Michielse S.
        • Schruers K.
        • et al.
        From laboratory to life: Associating brain reward processing with real-life motivated behaviour and symptoms of depression in non-help-seeking young adults.
        Psychol Med. 2019; 49: 2441-2451
        • Frank G.K.W.
        • DeGuzman M.C.
        • Shott M.E.
        • Laudenslager M.L.
        • Rossi B.
        • Pryor T.
        Association of brain reward learning response with harm avoidance, weight gain, and hypothalamic effective connectivity in adolescent anorexia nervosa.
        JAMA Psychiatry. 2018; 75: 1071-1080
        • Ernst M.
        • Romeo R.D.
        • Andersen S.L.
        Neurobiology of the development of motivated behaviors in adolescence: A window into a neural systems model.
        Pharmacol Biochem Behav. 2009; 93: 199-211
        • Fairchild G.
        The developmental psychopathology of motivation in adolescence.
        Dev Cogn Neurosci. 2011; 1: 414-429
        • Schultz W.
        Reward prediction error.
        Curr Biol. 2017; 27: R369-R371
        • Calkins S.D.
        • Dollar J.M.
        • Wideman L.
        Temperamental vulnerability to emotion dysregulation and risk for mental and physical health challenges.
        Dev Psychopathol. 2019; 31: 957-970
        • Keren H.
        • Chen G.
        • Benson B.
        • Ernst M.
        • Leibenluft E.
        • Fox N.A.
        • et al.
        Is the encoding of reward prediction error reliable during development?.
        Neuroimage. 2018; 178: 266-276
        • Garcia D.
        • Lundström S.
        • Brändström S.
        • Råstam M.
        • Cloninger C.R.
        • Kerekes N.
        • et al.
        Temperament and character in the Child and Adolescent Twin Study in Sweden (CATSS): Comparison to the general population, and genetic structure analysis.
        PLoS One. 2013; 8e70475
        • Geier C.
        • Luna B.
        The maturation of incentive processing and cognitive control.
        Pharmacol Biochem Behav. 2009; 93: 212-221
        • Cloninger C.R.
        • Cloninger K.M.
        • Zwir I.
        • Keltikangas-Järvinen L.
        The complex genetics and biology of human temperament: A review of traditional concepts in relation to new molecular findings.
        Transl Psychiatry. 2019; 9: 290
        • White L.K.
        • McDermott J.M.
        • Degnan K.A.
        • Henderson H.A.
        • Fox N.A.
        Behavioral inhibition and anxiety: The moderating roles of inhibitory control and attention shifting.
        J Abnorm Child Psychol. 2011; 39: 735-747
        • Wessman J.
        • Schönauer S.
        • Miettunen J.
        • Turunen H.
        • Parviainen P.
        • Seppänen J.K.
        • et al.
        Temperament clusters in a normal population: Implications for health and disease.
        PLoS One. 2012; 7e33088
        • Kim S.H.
        • Yoon H.
        • Kim H.
        • Hamann S.
        Individual differences in sensitivity to reward and punishment and neural activity during reward and avoidance learning.
        Soc Cogn Affect Neurosci. 2015; 10: 1219-1227
        • Panek-Scarborough L.M.
        • Dewey A.M.
        • Temple J.L.
        Sensation and perception of sucrose and fat stimuli predict the reinforcing value of food.
        Physiol Behav. 2012; 105: 1242-1249
        • Sheehan D.V.
        • Sheehan K.H.
        • Shytle R.D.
        • Janavs J.
        • Bannon Y.
        • Rogers J.E.
        • et al.
        Reliability and validity of the Mini International Neuropsychiatric Interview for Children and Adolescents (MINI-KID).
        J Clin Psychiatry. 2010; 71: 313-326
        • Cloninger C.R.
        • Przybeck T.R.
        • Svrakic D.M.
        • Wetzel R.D.
        The Temperament and Character Inventory (TCI): A Guide to Its Development and Use.
        Center for Psychobiology of Personality, Washington University, St Louis, MO1994
        • Torrubia R.
        • Ávila C.
        • Moltó J.
        • Caseras X.
        The Sensitivity to Punishment and Sensitivity to Reward Questionnaire (SPSRQ) as a measure of Gray’s anxiety and impulsivity dimensions.
        Pers Individ Dif. 2001; 31: 837-862
        • O’Doherty J.P.
        • Dayan P.
        • Friston K.
        • Critchley H.
        • Dolan R.J.
        Temporal difference models and reward-related learning in the human brain.
        Neuron. 2003; 38: 329-337
        • Frank G.K.
        • Kaye W.H.
        • Carter C.S.
        • Brooks S.
        • May C.
        • Fissell K.
        • Stenger V.A.
        The evaluation of brain activity in response to taste stimuli—A pilot study and method for central taste activation as assessed by event-related fMRI.
        J Neurosci Methods. 2003; 131: 99-105
        • Frank G.K.
        • Reynolds J.R.
        • Shott M.E.
        • Jappe L.
        • Yang T.T.
        • Tregellas J.R.
        • O’Reilly R.C.
        Anorexia nervosa and obesity are associated with opposite brain reward response.
        Neuropsychopharmacology. 2012; 37: 2031-2046
        • DeGuzman M.
        • Shott M.E.
        • Yang T.T.
        • Riederer J.
        • Frank G.K.W.
        Association of elevated reward prediction error response with weight gain in adolescent anorexia nervosa.
        Am J Psychiatry. 2017; 174: 557-565
        • O’Doherty J.P.
        • Hampton A.
        • Kim H.
        Model-based fMRI and its application to reward learning and decision making.
        Ann N Y Acad Sci. 2007; 1104: 35-53
        • Tzourio-Mazoyer N.
        • Landeau B.
        • Papathanassiou D.
        • Crivello F.
        • Etard O.
        • Delcroix N.
        • et al.
        Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.
        Neuroimage. 2002; 15: 273-289
        • O’Doherty J.
        • Dayan P.
        • Schultz J.
        • Deichmann R.
        • Friston K.
        • Dolan R.J.
        Dissociable roles of ventral and dorsal striatum in instrumental conditioning.
        Science. 2004; 304: 452-454
        • Breiter H.C.
        • Gollub R.L.
        • Weisskoff R.M.
        • Kennedy D.N.
        • Makris N.
        • Berke J.D.
        • et al.
        Acute effects of cocaine on human brain activity and emotion.
        Neuron. 1997; 19: 591-611
        • Benjamini Y.
        • Hochberg Y.
        Controlling the false discovery rate: A practical and powerful approach to multiple testing.
        J R Stat Soc B. 1995; 57: 289-300
        • Westfall P.H.
        On using the bootstrap for multiple comparisons.
        J Biopharm Stat. 2011; 21: 1187-1205
        • Kelley A.E.
        • Schochet T.
        • Landry C.F.
        Risk taking and novelty seeking in adolescence: Introduction to part I.
        Ann N Y Acad Sci. 2004; 1021: 27-32
        • Gusnard D.A.
        • Ollinger J.M.
        • Shulman G.L.
        • Cloninger C.R.
        • Price J.L.
        • Van Essen D.C.
        • Raichle M.E.
        Persistence and brain circuitry.
        Proc Natl Acad Sci U S A. 2003; 100: 3479-3484
        • Atiye M.
        • Miettunen J.
        • Raevuori-Helkamaa A.
        A meta-analysis of temperament in eating disorders.
        Eur Eat Disord Rev. 2015; 23: 89-99
        • Rosenström T.
        • Jylhä P.
        • Robert Cloninger C.
        • Hintsanen M.
        • Elovainio M.
        • Mantere O.
        • et al.
        Temperament and character traits predict future burden of depression.
        J Affect Disord. 2014; 158: 139-147
        • Hansenne M.
        • Bianchi J.
        Emotional intelligence and personality in major depression: Trait versus state effects.
        Psychiatry Res. 2009; 166: 63-68
        • Jakšić N.
        • Aukst-Margetić B.
        • Marčinko D.
        • Brajković L.
        • Lončar M.
        • Jakovljević M.
        Temperament, character, and suicidality among Croatian war veterans with posttraumatic stress disorder.
        Psychiatr Danub. 2015; 27: 60-63
        • Guyer A.E.
        • Benson B.
        • Choate V.R.
        • Bar-Haim Y.
        • Perez-Edgar K.
        • Jarcho J.M.
        • et al.
        Lasting associations between early-childhood temperament and late-adolescent reward-circuitry response to peer feedback.
        Dev Psychopathol. 2014; 26: 229-243
        • Schultz W.
        Neural coding of basic reward terms of animal learning theory, game theory, microeconomics and behavioural ecology.
        Curr Opin Neurobiol. 2004; 14: 139-147
        • Vidal-Ribas P.
        • Benson B.
        • Vitale A.D.
        • Keren H.
        • Harrewijn A.
        • Fox N.A.
        • et al.
        Bidirectional associations between stress and reward processing in children and adolescents: A longitudinal neuroimaging study.
        Biol Psychiatry Cogn Neurosci Neuroimaging. 2019; 4: 893-901
        • Zald D.H.
        • Treadway M.T.
        Reward processing, neuroeconomics, and psychopathology.
        Annu Rev Clin Psychol. 2017; 13: 471-495
        • Muscatell K.A.
        Socioeconomic influences on brain function: Implications for health.
        Ann N Y Acad Sci. 2018; 1428: 14-32
        • Grady C.L.
        • Rieck J.R.
        • Nichol D.
        • Rodrigue K.M.
        • Kennedy K.M.
        Influence of sample size and analytic approach on stability and interpretation of brain-behavior correlations in task-related fMRI data.
        Hum Brain Mapp. 2021; 42: 204-219
        • Diederen K.M.J.
        • Fletcher P.C.
        Dopamine, prediction error and beyond.
        Neuroscientist. 2021; 27: 30-46
        • Schultz W.
        Recent advances in understanding the role of phasic dopamine activity.
        F1000Res. 2019; 8 (Faculty Rev-1680): F1000
        • Haarsma J.
        • Fletcher P.C.
        • Griffin J.D.
        • Taverne H.J.
        • Ziauddeen H.
        • Spencer T.J.
        • et al.
        Precision weighting of cortical unsigned prediction error signals benefits learning, is mediated by dopamine, and is impaired in psychosis [published correction appears in Mol Psychiatry 2021; 26:5334]..
        Mol Psychiatry. 2021; 26: 5320-5333
        • Roesch M.R.
        • Calu D.J.
        • Esber G.R.
        • Schoenbaum G.
        All that glitters ... dissociating attention and outcome expectancy from prediction errors signals.
        J Neurophysiol. 2010; 104: 587-595