Aversive learning in adolescents: Modulation by amygdala-prefrontal and amygdala-hippocampal connectivity and neuroticism

Neuropsychopharmacology

Volumn 39, Issue 4, 2014, Pages 875-884

  Tzschoppe, Jelka ^a   Nees, Frauke ^a   Banaschewski, Tobias ^a   Barker, Gareth J ^b   Büchel, Christian ^c   Conrod, Patricia J ^b,d   Garavan, Hugh ^e   Heinz, Andreas ^f   Loth, Eva ^b   Mann, Karl ^a   Martinot, Jean Luc ^g,h   Smolka, Michael N ⁱ   Gallinat, Jürgen ^f   Ströhle, Aandreas ^f   Struve, Maren ^a   Rietschel, Marcella ^a   Schumann, Gunter ^b   Flor, Herta ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d UNIVERSITY OF MONTREAL   (Canada)

^e TRINITY COLLEGE DUBLIN   (Ireland)

^f CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^g INSERM   (France)

^h ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

ⁱ DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

adolescents; amygdale; hippocampus; neuroticism; pavlovian fear conditioning; prefrontal cortex

Indexed keywords

ADOLESCENT; AMYGDALA; ANXIETY DISORDERS; AVOIDANCE LEARNING; CONDITIONING, CLASSICAL; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; OXYGEN; PERSONALITY INVENTORY; PREFRONTAL CORTEX; PSYCHOPHYSICS;

EID: 84894097605     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.287     Document Type: Article

References (68)

1. Banks SJ, Eddy KT, Angstadt M, Nathan PJ, Phan KL (2007). Amygdala-frontal connectivity during emotion regulation. Soc Cogn Affect Neurosci 2: 303-312.
2. Baumgartner T, Knoch D, Hotz P, Eisenegger C, Fehr E (2011). Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice. Nat Neurosci 14: 1468-1474.
3. Benetti S, Mechelli A, Picchioni M, Broome M, Williams S, McGuire P (2009). Functional integration between the posterior hippocampus and prefrontal cortex is impaired in both first episode schizophrenia and the at risk mental state. Brain 132: 2426-2436.
4. Bradley M, Lang P (1999). International affective digitized sounds (IADS). edn University of Florida: Gainesville, FL, USA.
5. Bradley MM, Lang PJ (1994). Measuring emotion: the selfassessment manikin and the semantic differential. J Behav Ther Exp Psychiatry 25: 49-59.
6. Brown SA, Tapert SF, Granholm E, Delis DC (2000). Neurocognitive functioning of adolescents: effects of protracted alcohol use. Alcohol Clin Exp Res 24: 164-171.
7. Buchel C, Dolan RJ (2000). Classical fear conditioning in functional neuroimaging. Curr Opin Neurobiol 10: 219-223.
8. Canli T, Sivers H, Thomason ME, Whitfield-Gabrieli S, Gabrieli JD, Gotlib IH (2004). Brain activation to emotional words in depressed vs healthy subjects. Neuroreport 15: 2585-2588.
9. Canli T, Zhao Z, Desmond JE, Kang E, Gross J, Gabrieli JD (2001). An fMRI study of personality influences on Brain reactivity to emotional stimuli. Behav Neurosci 115: 33-42.
10. Compas BE, Orosan PG, Grant KE (1993). Adolescent stress and coping: implications for psychopathology during adolescence. J Adolesc 16: 331-349.
11. Costa PT Jr., McCrae RR (1997). Stability and change in personality assessment: the revised NEO personality inventory in the year 2000. J Pers Assess 68: 86-94.
12. Craske MG, Waters AM, Lindsey Bergman R, Naliboff B, Lipp OV, Negoro H et al (2008). Is aversive learning a marker of risk for anxiety disorders in children? Behav Res Ther 46: 954-967.
13. Craske MG, Waters AM, Nazarian M, Mineka S, Zinbarg RE, Griffith JW (2009). Does neuroticism in adolescents moderate contextual and explicit threat cue modulation of the startle reflex? Biol Psychiatry 65: 220-226.
14. Craske MG, Wolitzky-Taylor KB, Mineka S, Zinbarg R, Waters AM, Vrshek-Schallhorn S et al (2012). Elevated responding to safe conditions as a specific risk factor for anxiety versus depressive disorders: evidence from a longitudinal investigation. J Abnorm Psychol 121: 315-324.
15. Cremers HR, Demenescu LR, Aleman A, Renken R, van Tol MJ, van der Wee NJ et al (2010). Neuroticism modulates amygdalaprefrontal connectivity in response to negative emotional facial expressions. Neuroimage 49: 963-970.
16. Cullen KR, Gee DG, Klimes-Dougan B, Gabbay V, Hulvershorn L, Mueller BA et al (2009). A preliminary study of functional connectivity in comorbid adolescent depression. Neurosci Lett 460: 227-231.
17. Dalla C, Shors TJ (2009). Sex differences in learning processes of classical and operant conditioning. Physiol Behav 97: 229-238.
18. Deichmann R, Gottfried JA, Hutton C, Turner R (2003). Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 19: 430-441.
19. Ekman P (1982). Emotion in the Human Face. Cambridge University Press: Cambridge, UK.
20. Ernst M, Fudge JL (2009). A developmental neurobiological model of motivated behavior: anatomy, connectivity and ontogeny of the triadic nodes. Neurosci Biobehav Rev 33: 367-382.
21. Ernst M, Nelson EE, Jazbec S, McClure EB, Monk CS, Leibenluft E et al (2005). Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents. Neuroimage 25: 1279-1291.
22. Etkin A, Egner T, Kalisch R (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15: 85-93.
23. Fair DA, Nigg JT, Iver S, Bathula D, Mills KL, Dosenbach NU (2012). Distinct neural signatures detected for ADHD subtypes after controlling for micro-movements in resting state functional connectivity MRI data. Front Syst Neurosci 6: 80.
24. Fanselow MS, Dong HW (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65: 7-19.
25. Fendt M, Fanselow MS (1999). The neuroanatomical and neurochemical basis of conditioned fear. Neurosci Biobehav Rev 23: 743-760.
26. Goodman R, Ford T, Richards H, Gatward R, Meltzer H (2000). The Development and well-being assessment: description and initial validation of an integrated assessment of child and adolescent psychopathology. J Child Psychol Psychiatry 41: 645-655.
27. Haas BW, Constable RT, Canli T (2008). Stop the sadness: neuroticism is associated with sustained medial prefrontal cortex response to emotional facial expressions. Neuroimage 42: 385-392.
28. Harenski CL, Kim SH, Hamann S (2009). Neuroticism and psychopathy predict brain activation during moral and nonmoral emotion regulation. Cogn Affect. Behav Neurosci 9: 1-15.
29. Heinz A, Braus DF, Smolka MN, Wrase J, Puls I, Hermann D et al (2005). Amygdala-prefrontal coupling depends on a genetic variation of the serotonin transporter. Nat Neurosci 8: 20-21.
30. Hooker CI, Verosky SC, Miyakawa A, Knight RT, D'Esposito M (2008). The influence of personality on neural mechanisms of observational fear and reward learning. Neuropsychologia 46: 2709-2724.
31. Hulvershorn LA, Cullen K, Anand A (2011). Toward dysfunctional connectivity: a review of neuroimaging findings in pediatric major depressive disorder. Brain Imaging Behav 5: 307-328.
32. Jorm AF, Christensen H, Henderson AS, Jacomb PA, Korten AE, Rodgers B (2000). Predicting anxiety and depression from personality: is there a synergistic effect of neuroticism and extraversion? J Abnorm Psychol 109: 145-149.
33. Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 62: 593-602.
34. Kienast T, Hariri AR, Schlagenhauf F, Wrase J, Sterzer P, Buchholz HG et al (2008). Dopamine in amygdala gates limbic processing of aversive stimuli in humans. Nat Neurosci 11: 1381-1382.
35. Kim JJ, Jung MW (2006). Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neurosci Biobehav Rev 30: 188-202.
36. Kim MJ, Loucks RA, Palmer AL, Brown AC, Solomon KM, Marchante AN et al (2011a). The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav Brain Res 223: 403-410.
37. Kim MJ, Gee DG, Loucks RA, Davis FC, Whalen PJ (2011b). Anxiety dissociates dorsal and ventral medial prefrontal cortex functional connectivity with the amygdala at rest. Cereb. Cortex 21: 1667-1673.
38. Knutson B, Fong GW, Adams CM, Varner JL, Hommer D (2001). Dissociation of reward anticipation and outcome with eventrelated fMRI. Neuroreport 12: 3683-3687.
39. LaBar KS, LeDoux JE, Spencer DD, Phelps EA (1995). Impaired fear conditioning following unilateral temporal lobectomy in humans. J Neurosci 15: 6846-6855.
40. Lau JY, Britton JC, Nelson EE, Angold A, Ernst M, Goldwin M et al (2011). Distinct neural signatures of threat learning in adolescents and adults. Proc Natl Acad Sci USA 108: 4500-4505.
41. LeDoux JE (2000). Emotion circuits in the brain. Annu Rev Neurosci 23: 155-184.
42. Liu CC, Crone NE, Franaszczuk PJ, Cheng DT, Schretlen DS, Lenz FA (2011). Fear conditioning is associated with dynamic directed functional interactions between and within the human amygdala, hippocampus, and frontal lobe. Neuroscience 189: 359-369.
43. Maier S, Szalkowski A, Kamphausen S, Perlov E, Feige B, Blechert J, Philipsen A, van Elst LT, Kalisch R, Tuscher O (2012). Clarifying the role of the rostral dmPFC/dACC in fear/ anxiety: learning, appraisal or expression? PLoS One 7: e50120.
44. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19: 1233-1239.
45. Malin EL, McGaugh JL (2006). Differential involvement of the hippocampus, anterior cingulate cortex, and basolateral amygdala in memory for context and footshock. Proc Natl Acad Sci USA 103: 1959-1963.
46. Marek R, Strobel C, Bredy TW, Sah P (2013). The amygdala and medial prefrontal cortex: partners in the fear circuit. J Physiol 591: 2381-2391.
47. Maren S (2008). Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats. Eur J Neurosci 28: 1661-1666.
48. McGue M, Iacono WG (2005). The association of early adolescent problem behavior with adult psychopathology. Am J Psychiatry 162: 1118-1124.
49. Meyer-Lindenberg A, Weinberger DR (2006). Intermediate phenotypes and genetic mechanisms of psychiatric disorders. Nat Rev Neurosci 7: 818-827.
50. Neumann DL, Waters AM, Westbury HR (2008). The use of an unpleasant sound as the unconditional stimulus in aversive Pavlovian conditioning experiments that involve children and adolescent participants. Behav Res Methods 40: 622-625.
51. Nielsen FA, Hansen LK (2002). Modeling of activation data in the BrainMap database: detection of outliers. Hum Brain Mapp 15: 146-156.
52. Nieuwenhuis IL, Takashima A (2011). The role of the ventromedial prefrontal cortex in memory consolidation. Behav Brain Res 218: 325-334.
53. Ormel J, Bastiaansen A, Riese H, Bos EH, Servaas M, Ellenbogen M et al (2013). The biological and psychological basis of neuroticism: Current status and future directions. Neurosci and Biobehav Reviews 37: 59-72.
54. Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski BA, Munoz KE, Kolachana BS et al (2005). 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat Neurosci 8: 828-834.
55. Phelps EA (2004). Human emotion and memory: interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 14: 198-202.
56. Quirk GJ, Russo GK, Barron JL, Lebron K (2000). The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J Neurosci 20: 6225-6231.
57. Robinson OJ, Charney DR, Overstreet C, Vytal K, Grillon C (2012). The adaptive threat bias in anxiety: amygdala-dorsomedial prefrontal cortex coupling and aversive amplification. Neuroimage 60: 523-529.
58. Roth M (2002). U berprufung der Anwendbarkeit des NEO-Funf- Faktoren Inventars (NEO-FFI) bei Jugendlichen im Alter zwischen 14 und 16 Jahren. Diagnostica 48: 59-67.
59. Satpute AB, Mumford JA, Naliboff BD, Poldrack RA (2012). Human anterior and posterior hippocampus respond distinctly to state and trait anxiety. Emotion 12: 58-68.
60. Schumann G, Loth E, Banaschewski T, Barbot A, Barker G, Buchel C et al (2010). The IMAGEN study: reinforcement-related behaviour in normal brain function and psychopathology. Mol Psychiatry 15: 1128-1139.
61. Sehlmeyer C, Schoning S, Zwitserlood P, Pfleiderer B, Kircher T, Arolt V, Konrad C (2009). Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS One 4: e5865.
62. Siegle GJ, Thompson W, Carter CS, Steinhauer SR, Thase ME (2007). Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biol Psychiatry 61: 198-209.
63. Somerville LH, Jones RM, Casey BJ (2010). A time of change: behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain Cogn 72: 124-133.
64. Stein JL, Wiedholz LM, Bassett DS, Weinberger DR, Zink CF, Mattay VS et al (2007). A validated network of effective amygdala connectivity. Neuroimage 36: 736-745.
65. Tang J, Ko S, Ding HK, Qiu CS, Calejesan AA, Zhuo M (2005). Pavlovian fear memory induced by activation in the anterior cingulate cortex. Mol Pain 1: 6.
66. Weisberg YJ, Deyoung CG, Hirsh JB (2011). Gender differences in personality across the ten aspects of the big five. Front Psychol 2: 178.
67. Wright CI, Williams D, Feczko E, Barrett LF, Dickerson BC, Schwartz CE et al (2006). Neuroanatomical correlates of extraversion and neuroticism. Cereb Cortex 16: 1809-1819.
68. Yurgelun-Todd DA, Killgore WD (2006). Fear-related activity in the prefrontal cortex increases with age during adolescence: a preliminary fMRI study. Neurosci Lett 406: 194-199.