A specific neural substrate predicting current and future impulsivity in young adults.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
received:
12
06
2020
accepted:
05
01
2021
revised:
16
12
2020
pubmed:
27
1
2021
medline:
1
2
2022
entrez:
26
1
2021
Statut:
ppublish
Résumé
Impulsivity (rash action with deleterious outcomes) is common to many psychiatric disorders. While some studies indicate altered amygdala and prefrontal cortical (PFC) activity associated with impulsivity, it remains unclear whether these patterns of neural activity are specific to impulsivity or common to a range of affective and anxiety symptoms. To elucidate neural markers specific to impulsivity, we aimed to differentiate patterns of amygdala-PFC activity and functional connectivity associated with impulsivity from those associated with affective and anxiety symptoms, and identify measures of this circuitry predicting future worsening of impulsivity. Using a face emotion processing task that reliably activates amygdala-PFC circuitry, neural activity and connectivity were assessed in a transdiagnostically-recruited sample of young adults, including healthy (N = 47) and treatment-seeking individuals (N = 67). Relationships were examined between neural measures and impulsivity, anhedonia, and affective and anxiety symptoms at baseline (N = 114), and at 6 months post scan (N = 30). Impulsivity, particularly negative urgency and lack of perseverance, was related to greater amygdala activity (beta = 0.82, p = 0.003; beta = 0.68, p = 0.004; respectively) and lower amygdala-medial PFC functional connectivity (voxels = 60, t
Identifiants
pubmed: 33495543
doi: 10.1038/s41380-021-01017-0
pii: 10.1038/s41380-021-01017-0
pmc: PMC8589683
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4919-4930Subventions
Organisme : NIMH NIH HHS
ID : R01 MH100041
Pays : United States
Organisme : NIMH NIH HHS
ID : R37 MH100041
Pays : United States
Organisme : NIMH NIH HHS
ID : T32 MH018951
Pays : United States
Informations de copyright
© 2021. The Author(s).
Références
Kessler RC, Berglund P, Demler O, Jin R, Walters EE. Lifetime prevalence and age-of-onset distributions’ of DSM-IV disorders in the national comorbidity survey replication. Arch Gen Psychiatry. 2005;62:593–602.
pubmed: 15939837
doi: 10.1001/archpsyc.62.6.593
SAMHSA. Results from the 2006 National Survey on Drug Use and Health: National Findings. Publication No. SMA 07-4293. Rockville, Md: DHHS; 2007.
Whiteside SP, Lynam DR. The five factor model and impulsivity: using a structural model of personality to understand impulsivity. Personal Individual Differ. 2001;30:669–89.
doi: 10.1016/S0191-8869(00)00064-7
Cyders MA, Smith GT, Spillane NS, Fischer S, Annus AM, Peterson C. Integration of impulsivity and positive mood to predict risky behavior: development and validation of a measure of positive urgency. Psychol Assess. 2007;19:107–18.
pubmed: 17371126
doi: 10.1037/1040-3590.19.1.107
Johnson SL, Elliott MV, Carver CS. Impulsive responses to positive and negative emotions: parallel neurocognitive correlates and their implications. Biol Psychiatry. 2020;87:338–49.
pubmed: 31668478
doi: 10.1016/j.biopsych.2019.08.018
Marissen MAE, Arnold N, Franken IHA. Anhedonia in borderline personality disorder and its relation to symptoms of impulsivity. Psychopathology. 2012;45:179–84.
pubmed: 22441143
doi: 10.1159/000330893
American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th ed. Washington, DC: American Psychiatric Association; 2013.
Hare TA, Tottenham N, Galvan A, Voss HU, Glover GH, Casey BJ. Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biol Psychiatry. 2008;63:927–34.
pubmed: 18452757
pmcid: 2664095
doi: 10.1016/j.biopsych.2008.03.015
Somerville LH, Jones RM, Casey BJ. A time of change: behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain Cogn. 2010;72:124–33.
pubmed: 19695759
doi: 10.1016/j.bandc.2009.07.003
Eshel N, Nelson EE, Blair RJ, Pine DS, Ernst M. Neural substrates of choice selection in adults and adolescents: Development of the ventrolateral prefrontal and anterior cingulate cortices. Neuropsychologia. 2007;45:1270–9.
pubmed: 17118409
doi: 10.1016/j.neuropsychologia.2006.10.004
Sousa SS, Amaro E, Crego A, Goncalves OF, Sampaio A. Developmental trajectory of the prefrontal cortex: a systematic review of diffusion tensor imaging studies. Brain Imaging Behav. 2018;12:1197–210.
pubmed: 28913594
doi: 10.1007/s11682-017-9761-4
Etkin A, Egner T, Kalisch R. Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci. 2011;15:85–93.
pubmed: 21167765
doi: 10.1016/j.tics.2010.11.004
Morawetz C, Bode S, Derntl B, Heekeren HR. The effect of strategies, goals and stimulus material on the neural mechanisms of emotion regulation: a meta-analysis of fMRI studies. Neurosci Biobehav Rev. 2017;72:111–28.
pubmed: 27894828
doi: 10.1016/j.neubiorev.2016.11.014
Luna B, Padmanabhan A, O’Hearn K. What has fMRI told us about the development of cognitive control through adolescence? Brain Cogn. 2010;72:101–13.
pubmed: 19765880
doi: 10.1016/j.bandc.2009.08.005
Aron AR, Robbins TW, Poldrack RA. Inhibitrion and the right inferior frontal cortex: one decade on. Trends Cogn Sci. 2014;18:177–85.
pubmed: 24440116
doi: 10.1016/j.tics.2013.12.003
Whiteside SP, Lynam DR, Miller JD, Reynolds SK. Validation of the UPPS impulsive behaviour scale: a four-factor model of impulsivity. Eur J Personal. 2005;19:559–74.
doi: 10.1002/per.556
Berg JM, Latzman RD, Bliwise NG, Lilienfeld SO. Parsing the heterogeneity of impulsivity: a meta-analytic review of the behavioral implications of the UPPS for psychopathology. Psychol Assess. 2015;27:1129–46.
pubmed: 25822833
doi: 10.1037/pas0000111
Cyders MA, Dzemidzic M, Eiler WJ, Coskunpinar A, Karyadi KA, Kareken DA. Negative urgency mediates the relationship between amygdala and orbitofrontal cortex activation to negative emotional stimuli and general risk-taking. Cereb Cortex. 2015;25:4094–102.
pubmed: 24904065
doi: 10.1093/cercor/bhu123
Chester DS, Lynam DR, Milich R, Powell DK, Andersen AH, DeWall CN. How do negative emotions impair self-control? A neural model of negative urgency. Neuroimage. 2016;132:43–50.
pubmed: 26892861
doi: 10.1016/j.neuroimage.2016.02.024
Albein-Urios N, Verdejo-Roman J, Asensio S, Soriano-Mas C, Martinez-Gonzalez JM, Verdejo-Garcia A. Re-appraisal of negative emotions in cocaine dependence: dysfunctional corticolimbic activation and connectivity. Addict Biol. 2014;19:415–26.
pubmed: 22978709
doi: 10.1111/j.1369-1600.2012.00497.x
Chase HW, Fournier JC, Bertocci MA, Greenberg T, Aslam H, Stiffler R, et al. A pathway linking reward circuitry, impulsive sensation-seeking and risky decision-making in young adults: identifying neural markers for new interventions. Transl Psychiatry. 2017;7:9.
doi: 10.1038/tp.2017.60
Wilbertz T, Deserno L, Horstmann A, Neumann J, Villringer A, Heinze HJ, et al. Response inhibition and its relation to multidimensional impulsivity. Neuroimage. 2014;103:241–8.
pubmed: 25241087
doi: 10.1016/j.neuroimage.2014.09.021
Kessler RC, Amminger GP, Aguilar-Gaxiola S, Alonso J, Lee S, Ustun TB. Age of onset of mental disorders: a review of recent literature. Curr Opin Psychiatry. 2007;20:359–64.
pubmed: 17551351
pmcid: 1925038
doi: 10.1097/YCO.0b013e32816ebc8c
Shin LM, Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology. 2010;35:169–91.
pubmed: 19625997
doi: 10.1038/npp.2009.83
Siegle GJ, Thompson W, Carter CS, Steinhauer SR, Thase ME. Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biol Psychiatry. 2007;61:198–209.
pubmed: 17027931
doi: 10.1016/j.biopsych.2006.05.048
Keedwell PA, Andrew C, Williams SCR, Brammer MJ, Phillips ML. The neural correlates of anhedonia in major depressive disorder. Biol Psychiatry. 2005;58:843–53.
pubmed: 16043128
doi: 10.1016/j.biopsych.2005.05.019
Chen CH, Suckling J, Lennox BR, Ooi C, Bullmore ET. A quantitative meta-analysis of fMRI studies in bipolar disorder. Bipolar Disord. 2011;13:1–15.
pubmed: 21320248
doi: 10.1111/j.1399-5618.2011.00893.x
Phillips M, Ladouceur C, Drevets W. A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry. 2008;13:833–57.
doi: 10.1038/mp.2008.65
Lawrence NS, Williams AM, Surguladze S, Giampietro V, Brammer MJ, Andrew C, et al. Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biol Psychiatry. 2004;55:578–87.
pubmed: 15013826
doi: 10.1016/j.biopsych.2003.11.017
Price JL, Drevets WC. Neural circuits underlying the pathophysiology of mood disorders. Trends Cogn Sci. 2012;16:61–71.
pubmed: 22197477
doi: 10.1016/j.tics.2011.12.011
Keedwell P, Drapier D, Surguladze S, Giampietro V, Brammer M, Phillips M. Neural markers of symptomatic improvement during antidepressant therapy in severe depression: subgenual cingulate and visual cortical responses to sad, but not happy, facial stimuli are correlated with changes in symptom score. J Psychopharmacol. 2009;23:775–88.
pubmed: 18635699
doi: 10.1177/0269881108093589
Victor TA, Furey ML, Fromm SJ, Ohman A, Drevets WC. Relationship between amygdala responses to masked faces and mood state and treatment in major depressive disorder. Arch Gen Psychiatry. 2010;67:1128–38.
pubmed: 21041614
pmcid: 3253452
doi: 10.1001/archgenpsychiatry.2010.144
Stein MB, Simmons AN, Feinstein JS, Paulus MP. Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. Am J Psychiatry. 2007;164:318–27.
pubmed: 17267796
doi: 10.1176/ajp.2007.164.2.318
Etkin A, Prater KE, Hoeft F, Menon V, Schatzberg AF. Failure of anterior cingulate activation and connectivity with the amygdala during implicit regulation of emotional processing in generalized anxiety disorder. Am J Psychiatry. 2010;167:545–54.
pubmed: 20123913
pmcid: 4367202
doi: 10.1176/appi.ajp.2009.09070931
Hilbert K, Lueken U, Beesdo-Baum K. Neural structures, functioning and connectivity in Generalized Anxiety Disorder and interaction with neuroendocrine systems: a systematic review. J Affect Disord. 2014;158:114–26.
pubmed: 24655775
doi: 10.1016/j.jad.2014.01.022
Harvey PO, Pruessner J, Czechowska Y, Lepage M. Individual differences in trait anhedonia: a structural and functional magnetic resonance imaging study in non-clinical subjects. Mol Psychiatry. 2007;12:767–75.
doi: 10.1038/sj.mp.4002021
Heller AS, Johnstone T, Shackman AJ, Light SN, Peterson MJ, Kolden GG, et al. Reduced capacity to sustain positive emotion in major depression reflects diminished maintenance of fronto-striatal brain activation. Proc Natl Acad Sci USA. 2009;106:22445–50.
pubmed: 20080793
pmcid: 2796908
doi: 10.1073/pnas.0910651106
Bertocci MA, Bebko G, Dwojak A, Iyengar S, Ladouceur CD, Fournier JC, et al. Longitudinal relationships among activity in attention redirection neural circuitry and symptom severity in youth. Biol Psychiatry Cogn Neurosci Neuroimaging. 2017;2:336–45.
pubmed: 28480336
pmcid: 5416876
Bertocci MA, Bebko G, Versace A, Fournier JC, Iyengar S, Olino T, et al. Predicting clinical outcome from reward circuitry function and white matter structure in behaviorally and emotionally dysregulated youth. Mol Psychiatry. 2016;21:1194–201.
pubmed: 26903272
pmcid: 4993633
doi: 10.1038/mp.2016.5
Eckstrand KL, Forbes EE, Bertocci MA, Chase HW, Greenberg T, Lockovich J, et al. Anhedonia reduction and the association between left ventral striatal reward response and 6-month improvement in life satisfaction among young adults. Jama Psychiatry. 2019;76:958–65.
pubmed: 31066876
pmcid: 6506875
doi: 10.1001/jamapsychiatry.2019.0864
Fusar-Poli P, Placentino A, Carletti F, Landi P, Allen P, Surguladze S, et al. Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci. 2009;34:418–32.
pubmed: 19949718
pmcid: 2783433
Greenberg T, Bertocci MA, Chase HW, Stiffler R, Aslam HA, Graur S, et al. Mediation by anxiety of the relationship between amygdala activity during emotion processing and poor quality of life in young adults. Transl Psychiatry. 2017;7:8.
doi: 10.1038/tp.2017.127
First MB, Williams JBW, Karg RS, Spitzer RL. Structured clinical interview for DSM-5 disorders—research version (SCID-5-RV, MAR 2014 revision). Arlington, VA: American Psychiatric Association; 2014.
Buckby JA, Yung AR, Cosgrave EM, Killackey EJ. Clinical utility of the mood and anxiety symptom questionnaire (MASQ) in a sample of young help-seekers. Bmc Psychiatry. 2007;7:7.
doi: 10.1186/1471-244X-7-50
Hamilton M. A rating scale for depression. J Neurol Neurosurg Psychiatry. 1960;23:56–62.
pubmed: 14399272
pmcid: 495331
doi: 10.1136/jnnp.23.1.56
Hamilton M. The assessment of anxiety-states by rating. vol. 32. British psychological soc, St Andrews house, 48 Princess Rd East, Leicester LE1 7DR, LEICS. England: British journal of medical psychology; 1959. pp. 50–5.
Young RC, Biggs JT, Ziegler VE, Meyer DA. Rating-scale for mania—reliability, validity and sensitivity. Br J Psychiatry. 1978;133:429–35.
pubmed: 728692
doi: 10.1192/bjp.133.5.429
Axelson DA, Birmaher B, Strober MA, Goldstein BI, Ha W, Gill MK, et al. Course of subthreshold bipolar disorder in youth: diagnostic progression from bipolar disorder not otherwise specified. J Am Acad Child Adolesc Psychiatry. 2011;50:1001–16.
pubmed: 21961775
pmcid: 3185249
doi: 10.1016/j.jaac.2011.07.005
Fournier JC, Keener MT, Almeida J, Kronhaus DM, Phillip ML. Amygdala and whole-brain activity to emotional faces distinguishes major depressive disorder and bipolar disorder. Bipolar Disord. 2013;15:741–52.
pubmed: 23911154
pmcid: 3864629
doi: 10.1111/bdi.12106
Friedman J, Hastie T, Tibshirani R. Regularization paths for generalized linear models via coordinate descent. J Stat Softw. 2010;33:1–22.
pubmed: 20808728
pmcid: 2929880
doi: 10.18637/jss.v033.i01
Holland PW, Welsch RE. Robust regression using iteratively re-weighted least-squares. Commun Stat Part A Theory Methods. 1977;6:813–27.
doi: 10.1080/03610927708827533
Fritsch V, Da Mota B, Loth E, Varoquauxa G, Banaschewski T, Barker GJ, et al. Robust regression for large-scale neuroimaging studies. Neuroimage. 2015;111:431–41.
pubmed: 25731989
doi: 10.1016/j.neuroimage.2015.02.048
Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Stat. 2001;29:1165–88.
doi: 10.1214/aos/1013699998
Uher R, Perlis RH, Placentino A, Dernovsek MZ, Henigsberg N, Mors O, et al. Self-report and clinician-rated measures of depression severity: can one replace the other? Depress Anxiety. 2012;29:1043–9.
pubmed: 22933451
pmcid: 3750710
doi: 10.1002/da.21993
McLaren DG, Ries ML, Xu GF, Johnson SC. A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. Neuroimage. 2012;61:1277–86.
pubmed: 22484411
doi: 10.1016/j.neuroimage.2012.03.068
Cisler JM, Bush K, Steele JS. A comparison of statistical methods for detecting context-modulated functional connectivity in fMRI. Neuroimage. 2014;84:1042–52.
pubmed: 24055504
doi: 10.1016/j.neuroimage.2013.09.018
Woo CW, Krishnan A, Wager TD. Cluster-extent based thresholding in fMRI analyses: pitfalls and recommendations. Neuroimage. 2014;91:412–9.
pubmed: 24412399
doi: 10.1016/j.neuroimage.2013.12.058
Eklund A, Nichols TE, Knutsson H. Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci USA. 2016;113:7900–5.
pubmed: 27357684
pmcid: 4948312
doi: 10.1073/pnas.1602413113
Hassel S, Almeida JRC, Kerr N, Nau S, Ladouceur CD, Fissell K, et al. Elevated striatal and decreased dorsolateral prefrontal cortical activity in response to emotional stimuli in euthymic bipolar disorder: no associations with psychotropic medication load. Bipolar Disord. 2008;10:916–27.
pubmed: 19594507
pmcid: 2711546
doi: 10.1111/j.1399-5618.2008.00641.x
Almeida JRC, Versace A, Hassel S, Kupfer DJ, Phillips ML. Elevated amygdala activity to sad facial expressions: a state marker of bipolar but not unipolar depression. Biol Psychiatry. 2010;67:414–21.
pubmed: 19931855
doi: 10.1016/j.biopsych.2009.09.027
Stringaris A, Goodman R. Longitudinal outcome of youth oppositionality: irritable, headstrong, and hurtful behaviors have distinctive predictions. J Am Acad Child Adolesc Psychiatry. 2009;48:404–12.
pubmed: 19318881
doi: 10.1097/CHI.0b013e3181984f30
Muhtadie L, Johnson SL, Carver CS, Gotlib IH, Ketter TA. A profile approach to impulsivity in bipolar disorder: the key role of strong emotions. Acta Psychiatr Scand. 2014;129:100–8.
pubmed: 23600731
doi: 10.1111/acps.12136
Swann AC, Lijffijt M, Lane SD, Steinberg JL, Moeller FG. Increased trait-like impulsivity and course of illness in bipolar disorder. Bipolar Disord. 2009;11:280–8.
pubmed: 19419385
pmcid: 2723745
doi: 10.1111/j.1399-5618.2009.00678.x
Momennejad I, Haynes JD. Human anterior prefrontal cortex encodes the ‘what’ and ‘when’ of future intentions. Neuroimage. 2012;61:139–48.
pubmed: 22418393
doi: 10.1016/j.neuroimage.2012.02.079
Ramnani N, Owen AM. Anterior prefrontal cortex: Insights into function from anatomy and neuroimaging. Nat Rev Neurosci. 2004;5:184–94.
pubmed: 14976518
doi: 10.1038/nrn1343
Phelps EA, Delgado MR, Nearing KI, LeDoux JE. Extinction learning in humans: role of the amygdala and vmPFC. Neuron. 2004;43:897–905.
pubmed: 15363399
doi: 10.1016/j.neuron.2004.08.042
Mendez-Bertolo C, Moratti S, Toledano R, Lopez-Sosa F, Martinez-Alvarez R, Mah YH, et al. A fast pathway for fear in human amygdala. Nat Neurosci. 2016;19:1041–9.
pubmed: 27294508
doi: 10.1038/nn.4324
Namburi P, Beyeler A, Yorozu S, Calhoon GG, Halbert SA, Wichmann R, et al. A circuit mechanism for differentiating positive and negative associations. Nature. 2015;520:675–8.
pubmed: 25925480
pmcid: 4418228
doi: 10.1038/nature14366
Ciocchi S, Herry C, Grenier F, Wolff SBE, Letzkus JJ, Vlachos I, et al. Encoding of conditioned fear in central amygdala inhibitory circuits. Nature. 2010;468:277–82.
pubmed: 21068837
doi: 10.1038/nature09559
Altshuler L, Bookheimer S, Proenza MA, Townsend J, Sabb F, Firestine A, et al. Increased amygdala activation during mania: A functional magnetic resonance imaging study. Am J Psychiatry. 2005;162:1211–3.
pubmed: 15930074
doi: 10.1176/appi.ajp.162.6.1211
Foland-Ross LC, Bookheimer SY, Lieberman MD, Sugar CA, Townsend JD, Fischer J, et al. Normal amygdala activation but deficient ventrolateral prefrontal activation in adults with bipolar disorder during euthymia. Neuroimage. 2012;59:738–44.
pubmed: 21854858
doi: 10.1016/j.neuroimage.2011.07.054
Vizueta N, Rudie JD, Townsend JD, Torrisi S, Moody TD, Bookheimer SY, et al. Regional fMRI hypoactivation and altered functional connectivity during emotion processing in nonmedicated depressed patients with bipolar II disorder. Am J Psychiatry. 2012;169:831–40.
pubmed: 22773540
pmcid: 3740182
doi: 10.1176/appi.ajp.2012.11030349
Soehner AM, Bertocci MA, Manelis A, Bebko G, Ladouceur CD, Graur S, et al. Preliminary investigation of the relationships between sleep duration, reward circuitry function, and mood dysregulation in youth offspring of parents with bipolar disorder. J Affect Disord. 2016;205:144–53.
pubmed: 27442458
pmcid: 5129838
doi: 10.1016/j.jad.2016.03.074