Healthy Adolescents' Neural Response to Reward: Associations With Puberty, Positive Affect, and Depressive Symptoms

Objective Changes in reward-related behavior are an important component of normal adolescent affective development. Understanding the neural underpinnings of these normative changes creates a foundation for investigating adolescence as a period of vulnerability to affective disorders, substance use...

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Veröffentlicht in:Journal of the American Academy of Child and Adolescent Psychiatry 2010-02, Vol.49 (2), p.162-172.e5
Hauptverfasser: Forbes, Erika E., Ph.D, Ryan, Neal D., M.D, Phillips, Mary L., M.D, Manuck, Stephen B., Ph.D, Worthman, Carol M., Ph.D, Moyles, Donna L., B.A, Tarr, Jill A., M.S.W, Sciarrillo, Samantha R., B.A, Dahl, Ronald E., M.D
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container_issue 2
container_start_page 162
container_title Journal of the American Academy of Child and Adolescent Psychiatry
container_volume 49
creator Forbes, Erika E., Ph.D
Ryan, Neal D., M.D
Phillips, Mary L., M.D
Manuck, Stephen B., Ph.D
Worthman, Carol M., Ph.D
Moyles, Donna L., B.A
Tarr, Jill A., M.S.W
Sciarrillo, Samantha R., B.A
Dahl, Ronald E., M.D
description Objective Changes in reward-related behavior are an important component of normal adolescent affective development. Understanding the neural underpinnings of these normative changes creates a foundation for investigating adolescence as a period of vulnerability to affective disorders, substance use disorders, and health problems. Studies of reward-related brain function have revealed conflicting findings regarding developmental change in the reactivity of the striatum and medial prefrontal cortex (mPFC) and have not considered puberty. The current study focused on puberty-specific changes in brain function and their association with mood. Method A sample of 77 healthy adolescents (26 pre-/early pubertal, 51 mid-/late pubertal) recruited in a narrow age range (mean = 11.94 years, SD = 0.75) were assessed for sexual maturation and circulating testosterone, completed a functional magnetic resonance imaging (fMRI) guessing task with monetary reward, and underwent experience sampling of mood in natural environments. For comparison, 19 healthy adults completed the fMRI assessment. Results Adolescents with more advanced pubertal maturation exhibited less striatal and more mPFC reactivity during reward outcome than similarly aged adolescents with less advanced maturation. Testosterone was positively correlated with striatal reactivity in boys during reward anticipation and negatively correlated with striatal reactivity in girls and boys during reward outcome. Striatal reactivity was positively correlated with real-world subjective positive affect and negatively correlated with depressive symptoms. mPFC reactivity was positively correlated with depressive symptoms. Conclusions Reward-related brain function changes with puberty and is associated with adolescents' positive affect and depressive symptoms. Increased reward-seeking behavior at this developmental point could serve to compensate for these changes.
doi_str_mv 10.1016/j.jaac.2009.11.006
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Understanding the neural underpinnings of these normative changes creates a foundation for investigating adolescence as a period of vulnerability to affective disorders, substance use disorders, and health problems. Studies of reward-related brain function have revealed conflicting findings regarding developmental change in the reactivity of the striatum and medial prefrontal cortex (mPFC) and have not considered puberty. The current study focused on puberty-specific changes in brain function and their association with mood. Method A sample of 77 healthy adolescents (26 pre-/early pubertal, 51 mid-/late pubertal) recruited in a narrow age range (mean = 11.94 years, SD = 0.75) were assessed for sexual maturation and circulating testosterone, completed a functional magnetic resonance imaging (fMRI) guessing task with monetary reward, and underwent experience sampling of mood in natural environments. For comparison, 19 healthy adults completed the fMRI assessment. Results Adolescents with more advanced pubertal maturation exhibited less striatal and more mPFC reactivity during reward outcome than similarly aged adolescents with less advanced maturation. Testosterone was positively correlated with striatal reactivity in boys during reward anticipation and negatively correlated with striatal reactivity in girls and boys during reward outcome. Striatal reactivity was positively correlated with real-world subjective positive affect and negatively correlated with depressive symptoms. mPFC reactivity was positively correlated with depressive symptoms. Conclusions Reward-related brain function changes with puberty and is associated with adolescents' positive affect and depressive symptoms. Increased reward-seeking behavior at this developmental point could serve to compensate for these changes.</description><identifier>ISSN: 0890-8567</identifier><identifier>EISSN: 1527-5418</identifier><identifier>DOI: 10.1016/j.jaac.2009.11.006</identifier><identifier>PMID: 20215938</identifier><identifier>CODEN: JAAPEE</identifier><language>eng</language><publisher>Maryland Heights, MO: Elsevier Inc</publisher><subject>Adolescent ; Adolescents ; Adult ; Adult and adolescent clinical studies ; Adults ; Affect - physiology ; Behavior ; Biological and medical sciences ; Brain ; Brain function ; Child ; Child clinical studies ; Child development ; Cognitive Development ; Comparative Analysis ; Corpus Striatum - physiopathology ; Correlation ; Cortex ; Depression ; Depression (Psychology) ; Depression - diagnosis ; Depression - physiopathology ; Development ; Evaluation Methods ; Evoked Potentials - physiology ; Female ; Females ; Guessing (Tests) ; Humans ; Image Processing, Computer-Assisted ; Investigations ; Magnetic Resonance Imaging ; Male ; Males ; Maturation ; Medical sciences ; Mental depression ; Mood disorders ; Motivation ; Pediatrics ; Personality Inventory - statistics &amp; numerical data ; Positive affect ; Prefrontal Cortex - physiopathology ; Psychiatry ; Psychology. Psychoanalysis. Psychiatry ; Psychometrics ; Psychopathology. Psychiatry ; Puberty ; Puberty - physiology ; Reactivity ; Reward ; Rewards ; Science Education ; Task Analysis ; Teenagers ; Testosterone - blood</subject><ispartof>Journal of the American Academy of Child and Adolescent Psychiatry, 2010-02, Vol.49 (2), p.162-172.e5</ispartof><rights>American Academy of Child and Adolescent Psychiatry</rights><rights>2010 American Academy of Child and Adolescent Psychiatry</rights><rights>2015 INIST-CNRS</rights><rights>Copyright Lippincott Williams &amp; Wilkins Feb 2010</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c538t-97efe69b5243cba764298d18ae5ac630ff5b7a7b262049f3ded04435d7d663223</citedby><cites>FETCH-LOGICAL-c538t-97efe69b5243cba764298d18ae5ac630ff5b7a7b262049f3ded04435d7d663223</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0890856709000240$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,776,780,881,3537,27903,27904,30978,30979,65309</link.rule.ids><backlink>$$Uhttp://eric.ed.gov/ERICWebPortal/detail?accno=EJ944741$$DView record in ERIC$$Hfree_for_read</backlink><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=22445718$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20215938$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Forbes, Erika E., Ph.D</creatorcontrib><creatorcontrib>Ryan, Neal D., M.D</creatorcontrib><creatorcontrib>Phillips, Mary L., M.D</creatorcontrib><creatorcontrib>Manuck, Stephen B., Ph.D</creatorcontrib><creatorcontrib>Worthman, Carol M., Ph.D</creatorcontrib><creatorcontrib>Moyles, Donna L., B.A</creatorcontrib><creatorcontrib>Tarr, Jill A., M.S.W</creatorcontrib><creatorcontrib>Sciarrillo, Samantha R., B.A</creatorcontrib><creatorcontrib>Dahl, Ronald E., M.D</creatorcontrib><title>Healthy Adolescents' Neural Response to Reward: Associations With Puberty, Positive Affect, and Depressive Symptoms</title><title>Journal of the American Academy of Child and Adolescent Psychiatry</title><addtitle>J Am Acad Child Adolesc Psychiatry</addtitle><description>Objective Changes in reward-related behavior are an important component of normal adolescent affective development. Understanding the neural underpinnings of these normative changes creates a foundation for investigating adolescence as a period of vulnerability to affective disorders, substance use disorders, and health problems. Studies of reward-related brain function have revealed conflicting findings regarding developmental change in the reactivity of the striatum and medial prefrontal cortex (mPFC) and have not considered puberty. The current study focused on puberty-specific changes in brain function and their association with mood. Method A sample of 77 healthy adolescents (26 pre-/early pubertal, 51 mid-/late pubertal) recruited in a narrow age range (mean = 11.94 years, SD = 0.75) were assessed for sexual maturation and circulating testosterone, completed a functional magnetic resonance imaging (fMRI) guessing task with monetary reward, and underwent experience sampling of mood in natural environments. For comparison, 19 healthy adults completed the fMRI assessment. Results Adolescents with more advanced pubertal maturation exhibited less striatal and more mPFC reactivity during reward outcome than similarly aged adolescents with less advanced maturation. Testosterone was positively correlated with striatal reactivity in boys during reward anticipation and negatively correlated with striatal reactivity in girls and boys during reward outcome. Striatal reactivity was positively correlated with real-world subjective positive affect and negatively correlated with depressive symptoms. mPFC reactivity was positively correlated with depressive symptoms. Conclusions Reward-related brain function changes with puberty and is associated with adolescents' positive affect and depressive symptoms. Increased reward-seeking behavior at this developmental point could serve to compensate for these changes.</description><subject>Adolescent</subject><subject>Adolescents</subject><subject>Adult</subject><subject>Adult and adolescent clinical studies</subject><subject>Adults</subject><subject>Affect - physiology</subject><subject>Behavior</subject><subject>Biological and medical sciences</subject><subject>Brain</subject><subject>Brain function</subject><subject>Child</subject><subject>Child clinical studies</subject><subject>Child development</subject><subject>Cognitive Development</subject><subject>Comparative Analysis</subject><subject>Corpus Striatum - physiopathology</subject><subject>Correlation</subject><subject>Cortex</subject><subject>Depression</subject><subject>Depression (Psychology)</subject><subject>Depression - diagnosis</subject><subject>Depression - physiopathology</subject><subject>Development</subject><subject>Evaluation Methods</subject><subject>Evoked Potentials - physiology</subject><subject>Female</subject><subject>Females</subject><subject>Guessing (Tests)</subject><subject>Humans</subject><subject>Image Processing, Computer-Assisted</subject><subject>Investigations</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Males</subject><subject>Maturation</subject><subject>Medical sciences</subject><subject>Mental depression</subject><subject>Mood disorders</subject><subject>Motivation</subject><subject>Pediatrics</subject><subject>Personality Inventory - statistics &amp; numerical data</subject><subject>Positive affect</subject><subject>Prefrontal Cortex - physiopathology</subject><subject>Psychiatry</subject><subject>Psychology. 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Psychiatry</subject><subject>Puberty</subject><subject>Puberty - physiology</subject><subject>Reactivity</subject><subject>Reward</subject><subject>Rewards</subject><subject>Science Education</subject><subject>Task Analysis</subject><subject>Teenagers</subject><subject>Testosterone - blood</subject><issn>0890-8567</issn><issn>1527-5418</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>7QJ</sourceid><recordid>eNp9kl-L00AUxYMobq1-AREJgqwP2zp_MxORhbKurrLo4io-DtPJjZ2aZurcpNJv74TWqvuwTxlyfvdw7z03yx5TMqWEFi-X06W1bsoIKaeUTgkp7mQjKpmaSEH13WxEdEkmWhbqKHuAuCSEUKX1_eyIEUZlyfUowwuwTbfY5rMqNIAO2g6P84_QR9vknwHXoUXIu5Dev2ysXuUzxOC87XwS8m--W-RX_Rxitz3JrwL6zm8gn9U1uO4kt22Vv4F1BMTh9_V2te7CCh9m92rbIDzaf8fZ17fnX84uJpef3r0_m11OnOS6m5QKaijKuWSCu7lVhWClrqi2IK0rOKlrOVdWzVnBiChrXkFFhOCyUlVRcMb4ODvd-a77-QqqYbY0lVlHv7Jxa4L15n-l9QvzPWwM01xJWSSD471BDD97wM6sfFpR09gWQo9GSaEV5YVM5ItbSUqZTK4lHUyf3UCXoY9tWoRhidKcpiHGGdtBLgbECPWha0rMEL5ZmiF8M4Sf3E0KPxU9_XfeQ8mftBPwfA9YdLapo22dx78cE0IqOnBPdhxE7w7y-YdSCCVokl_v5RTexkM06Dy0DiofU-6mCv72Nk9vlLvGtz419AO2gIdtUIPMEHM9XPFwxKRMB8wE4b8BwhPrsA</recordid><startdate>20100201</startdate><enddate>20100201</enddate><creator>Forbes, Erika E., Ph.D</creator><creator>Ryan, Neal D., M.D</creator><creator>Phillips, Mary L., M.D</creator><creator>Manuck, Stephen B., Ph.D</creator><creator>Worthman, Carol M., Ph.D</creator><creator>Moyles, Donna L., B.A</creator><creator>Tarr, Jill A., M.S.W</creator><creator>Sciarrillo, Samantha R., B.A</creator><creator>Dahl, Ronald E., M.D</creator><general>Elsevier Inc</general><general>Elsevier</general><general>Elsevier BV</general><scope>7SW</scope><scope>BJH</scope><scope>BNH</scope><scope>BNI</scope><scope>BNJ</scope><scope>BNO</scope><scope>ERI</scope><scope>PET</scope><scope>REK</scope><scope>WWN</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QJ</scope><scope>7TK</scope><scope>K9.</scope><scope>5PM</scope></search><sort><creationdate>20100201</creationdate><title>Healthy Adolescents' Neural Response to Reward: Associations With Puberty, Positive Affect, and Depressive Symptoms</title><author>Forbes, Erika E., Ph.D ; Ryan, Neal D., M.D ; Phillips, Mary L., M.D ; Manuck, Stephen B., Ph.D ; Worthman, Carol M., Ph.D ; Moyles, Donna L., B.A ; Tarr, Jill A., M.S.W ; Sciarrillo, Samantha R., B.A ; Dahl, Ronald E., M.D</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c538t-97efe69b5243cba764298d18ae5ac630ff5b7a7b262049f3ded04435d7d663223</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Adolescent</topic><topic>Adolescents</topic><topic>Adult</topic><topic>Adult and adolescent clinical studies</topic><topic>Adults</topic><topic>Affect - physiology</topic><topic>Behavior</topic><topic>Biological and medical sciences</topic><topic>Brain</topic><topic>Brain function</topic><topic>Child</topic><topic>Child clinical studies</topic><topic>Child development</topic><topic>Cognitive Development</topic><topic>Comparative Analysis</topic><topic>Corpus Striatum - physiopathology</topic><topic>Correlation</topic><topic>Cortex</topic><topic>Depression</topic><topic>Depression (Psychology)</topic><topic>Depression - diagnosis</topic><topic>Depression - physiopathology</topic><topic>Development</topic><topic>Evaluation Methods</topic><topic>Evoked Potentials - physiology</topic><topic>Female</topic><topic>Females</topic><topic>Guessing (Tests)</topic><topic>Humans</topic><topic>Image Processing, Computer-Assisted</topic><topic>Investigations</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Males</topic><topic>Maturation</topic><topic>Medical sciences</topic><topic>Mental depression</topic><topic>Mood disorders</topic><topic>Motivation</topic><topic>Pediatrics</topic><topic>Personality Inventory - statistics &amp; numerical data</topic><topic>Positive affect</topic><topic>Prefrontal Cortex - physiopathology</topic><topic>Psychiatry</topic><topic>Psychology. Psychoanalysis. Psychiatry</topic><topic>Psychometrics</topic><topic>Psychopathology. Psychiatry</topic><topic>Puberty</topic><topic>Puberty - physiology</topic><topic>Reactivity</topic><topic>Reward</topic><topic>Rewards</topic><topic>Science Education</topic><topic>Task Analysis</topic><topic>Teenagers</topic><topic>Testosterone - blood</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Forbes, Erika E., Ph.D</creatorcontrib><creatorcontrib>Ryan, Neal D., M.D</creatorcontrib><creatorcontrib>Phillips, Mary L., M.D</creatorcontrib><creatorcontrib>Manuck, Stephen B., Ph.D</creatorcontrib><creatorcontrib>Worthman, Carol M., Ph.D</creatorcontrib><creatorcontrib>Moyles, Donna L., B.A</creatorcontrib><creatorcontrib>Tarr, Jill A., M.S.W</creatorcontrib><creatorcontrib>Sciarrillo, Samantha R., B.A</creatorcontrib><creatorcontrib>Dahl, Ronald E., M.D</creatorcontrib><collection>ERIC</collection><collection>ERIC (Ovid)</collection><collection>ERIC</collection><collection>ERIC</collection><collection>ERIC (Legacy Platform)</collection><collection>ERIC( SilverPlatter )</collection><collection>ERIC</collection><collection>ERIC PlusText (Legacy Platform)</collection><collection>Education Resources Information Center (ERIC)</collection><collection>ERIC</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Applied Social Sciences Index &amp; Abstracts (ASSIA)</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of the American Academy of Child and Adolescent Psychiatry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Forbes, Erika E., Ph.D</au><au>Ryan, Neal D., M.D</au><au>Phillips, Mary L., M.D</au><au>Manuck, Stephen B., Ph.D</au><au>Worthman, Carol M., Ph.D</au><au>Moyles, Donna L., B.A</au><au>Tarr, Jill A., M.S.W</au><au>Sciarrillo, Samantha R., B.A</au><au>Dahl, Ronald E., M.D</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><ericid>EJ944741</ericid><atitle>Healthy Adolescents' Neural Response to Reward: Associations With Puberty, Positive Affect, and Depressive Symptoms</atitle><jtitle>Journal of the American Academy of Child and Adolescent Psychiatry</jtitle><addtitle>J Am Acad Child Adolesc Psychiatry</addtitle><date>2010-02-01</date><risdate>2010</risdate><volume>49</volume><issue>2</issue><spage>162</spage><epage>172.e5</epage><pages>162-172.e5</pages><issn>0890-8567</issn><eissn>1527-5418</eissn><coden>JAAPEE</coden><abstract>Objective Changes in reward-related behavior are an important component of normal adolescent affective development. Understanding the neural underpinnings of these normative changes creates a foundation for investigating adolescence as a period of vulnerability to affective disorders, substance use disorders, and health problems. Studies of reward-related brain function have revealed conflicting findings regarding developmental change in the reactivity of the striatum and medial prefrontal cortex (mPFC) and have not considered puberty. The current study focused on puberty-specific changes in brain function and their association with mood. Method A sample of 77 healthy adolescents (26 pre-/early pubertal, 51 mid-/late pubertal) recruited in a narrow age range (mean = 11.94 years, SD = 0.75) were assessed for sexual maturation and circulating testosterone, completed a functional magnetic resonance imaging (fMRI) guessing task with monetary reward, and underwent experience sampling of mood in natural environments. For comparison, 19 healthy adults completed the fMRI assessment. Results Adolescents with more advanced pubertal maturation exhibited less striatal and more mPFC reactivity during reward outcome than similarly aged adolescents with less advanced maturation. Testosterone was positively correlated with striatal reactivity in boys during reward anticipation and negatively correlated with striatal reactivity in girls and boys during reward outcome. Striatal reactivity was positively correlated with real-world subjective positive affect and negatively correlated with depressive symptoms. mPFC reactivity was positively correlated with depressive symptoms. Conclusions Reward-related brain function changes with puberty and is associated with adolescents' positive affect and depressive symptoms. Increased reward-seeking behavior at this developmental point could serve to compensate for these changes.</abstract><cop>Maryland Heights, MO</cop><pub>Elsevier Inc</pub><pmid>20215938</pmid><doi>10.1016/j.jaac.2009.11.006</doi><tpages>11</tpages></addata></record>
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source Applied Social Sciences Index & Abstracts (ASSIA); MEDLINE; Elsevier ScienceDirect Journals
subjects Adolescent
Adolescents
Adult
Adult and adolescent clinical studies
Adults
Affect - physiology
Behavior
Biological and medical sciences
Brain
Brain function
Child
Child clinical studies
Child development
Cognitive Development
Comparative Analysis
Corpus Striatum - physiopathology
Correlation
Cortex
Depression
Depression (Psychology)
Depression - diagnosis
Depression - physiopathology
Development
Evaluation Methods
Evoked Potentials - physiology
Female
Females
Guessing (Tests)
Humans
Image Processing, Computer-Assisted
Investigations
Magnetic Resonance Imaging
Male
Males
Maturation
Medical sciences
Mental depression
Mood disorders
Motivation
Pediatrics
Personality Inventory - statistics & numerical data
Positive affect
Prefrontal Cortex - physiopathology
Psychiatry
Psychology. Psychoanalysis. Psychiatry
Psychometrics
Psychopathology. Psychiatry
Puberty
Puberty - physiology
Reactivity
Reward
Rewards
Science Education
Task Analysis
Teenagers
Testosterone - blood
title Healthy Adolescents' Neural Response to Reward: Associations With Puberty, Positive Affect, and Depressive Symptoms
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