Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-25T03:59:03.628Z Has data issue: false hasContentIssue false

Functional brain-imaging correlates of negative affectivity and the onset of first-episode depression

Published online by Cambridge University Press:  27 August 2014

C. G. Davey*
Affiliation:
Orygen Youth Health Research Centre, Centre for Youth Mental Health, The University of Melbourne, Parkville, Victoria, Australia Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne, Parkville, Victoria, Australia
S. Whittle
Affiliation:
Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne, Parkville, Victoria, Australia
B. J. Harrison
Affiliation:
Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne, Parkville, Victoria, Australia
J. G. Simmons
Affiliation:
Melbourne School of Psychological Sciences, The University of Melbourne, Parkville, Victoria, Australia
M. L. Byrne
Affiliation:
Melbourne School of Psychological Sciences, The University of Melbourne, Parkville, Victoria, Australia
O. S. Schwartz
Affiliation:
Melbourne School of Psychological Sciences, The University of Melbourne, Parkville, Victoria, Australia
N. B. Allen
Affiliation:
Melbourne School of Psychological Sciences, The University of Melbourne, Parkville, Victoria, Australia
*
*Address for correspondence: Dr C. G. Davey, Orygen Youth Health Research Centre, Centre for Youth Mental Health, The University of Melbourne, Parkville, Victoria 3052, Australia. (Email: c.davey@unimelb.edu.au)

Abstract

Background.

The amygdala and subgenual anterior cingulate cortex (sACC) are key brain regions for the generation of negative affect. In this longitudinal fMRI study of adolescents we investigated how amygdala–sACC connectivity was correlated with negative affectivity (NA) both cross-sectionally and longitudinally, and examined its relationship to the onset of first-episode depression.

Method.

Fifty-six adolescents who were part of a larger longitudinal study of adolescent development were included. They had no history of mental illness at the time of their baseline scan (mean age 16.5 years) and had a follow-up scan 2 years later (mean age 18.8 years). We used resting-state functional-connectivity MRI to investigate whether cross-sectional and change measures of amygdala–sACC connectivity were (i) correlated with NA and its change over time, and (ii) related to the onset of first-episode depression.

Results.

The magnitude of amygdala connectivity with sACC showed significant positive correlation with NA at both time-points. Further analysis confirmed that change in amygdala–sACC connectivity between assessments was correlated with change in NA. Eight participants developed a first episode of depression between the baseline and follow-up assessments: they showed increased amygdala–sACC connectivity at follow-up.

Conclusions.

Amygdala–sACC connectivity is associated with NA in adolescence, with change in connectivity between these regions showing positive correlation with change in NA. Our observation that the onset of depression was associated with an increase in connectivity between the regions provides support for the neurobiological ‘scar’ hypothesis of depression.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adolphs, R (2010). What does the amygdala contribute to social cognition? Annals of the New York Academy of Sciences 1191, 4261.CrossRefGoogle ScholarPubMed
Almeida, JR, Kronhaus, DM, Sibille, EL, Langenecker, SA, Versace, A, Labarbara, EJ, Phillips, ML (2011). Abnormal left-sided orbitomedial prefrontal cortical-amygdala connectivity during happy and fear face processing: a potential neural mechanism of female MDD. Frontiers in Psychiatry 2, 69.CrossRefGoogle ScholarPubMed
An, X, Bandler, R, Ongur, D, Price, JL (1998). Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys. Journal of Comparative Neurology 401, 455479.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Beckmann, M, Johansen-Berg, H, Rushworth, MF (2009). Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. Journal of Neuroscience 29, 11751190.CrossRefGoogle ScholarPubMed
Brown, BB (2004). Adolescents’ relationships with peers. In Handbook of Adolescent Psychology (ed. Lerner, R. M. and Steinberg, L. D.), pp. 363394. John Wiley & Sons: Hoboken, NJ.Google Scholar
Buckner, RL, Andrews-Hanna, JR, Schacter, DL (2008). The brain's default network: anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences 1124, 138.Google Scholar
Clark, LA, Watson, D, Mineka, S (1994). Temperament, personality, and the mood and anxiety disorders. Journal of Abnormal Psychology 103, 103116.CrossRefGoogle ScholarPubMed
Cloninger, CR, Przybeck, TR, Svrakic, DM (1991). The Tridimensional Personality Questionnaire: U.S. normative data. Psychological Reports 69, 10471057.CrossRefGoogle ScholarPubMed
Connolly, CG, Wu, J, Ho, TC, Hoeft, F, Wolkowitz, O, Eisendrath, S, Frank, G, Hendren, R, Max, JE, Paulus, MP, Tapert, SF, Banerjee, D, Simmons, AN, Yang, TT (2013). Resting-state functional connectivity of subgenual anterior cingulate cortex in depressed adolescents. Biological Psychiatry 74, 898907.Google Scholar
Craske, MG, Waters, AM, Nazarian, M, Mineka, S, Zinbarg, RE, Griffith, JW, Naliboff, B, Ornitz, EM (2009). Does neuroticism in adolescents moderate contextual and explicit threat cue modulation of the startle reflex? Biological Psychiatry 65, 220226.CrossRefGoogle ScholarPubMed
Cronbach, LJ, Furby, L (1970). How we should measure ‘change’: or should we? Psychological Bulletin 74, 6880.CrossRefGoogle Scholar
Cunningham, WA, Arbuckle, NL, Jahn, A, Mowrer, SM, Abduljalil, AM (2010). Aspects of neuroticism and the amygdala: chronic tuning from motivational styles. Neuropsychologia 48, 33993404.CrossRefGoogle ScholarPubMed
Ellis, LK, Rothbart, MK (2001). Revision of the Early Adolescent Temperament Questionnaire. Poster presented at the 2001 Biennial Meeting of the Society for Research in Child Development.Google Scholar
Fox, MD, Corbetta, M, Snyder, AZ, Vincent, JL, Raichle, ME (2006). Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proceedings of the National Academy of Sciences of the United States of America 103, 1004610051.CrossRefGoogle ScholarPubMed
Freedman, LJ, Insel, TR, Smith, Y (2000). Subcortical projections of area 25 (subgenual cortex) of the macaque monkey. Journal of Comparative Neurology 421, 172188.Google Scholar
Gotlib, IH, Sivers, H, Gabrieli, JD, Whitfield-Gabrieli, S, Goldin, P, Minor, KL, Canli, T (2005). Subgenual anterior cingulate activation to valenced emotional stimuli in major depression. Neuroreport 16, 17311734.Google Scholar
Haas, BW, Omura, K, Constable, RT, Canli, T (2007). Emotional conflict and neuroticism: personality-dependent activation in the amygdala and subgenual anterior cingulate. Behavioral Neuroscience 121, 249256.Google Scholar
Harrison, BJ, Soriano-Mas, C, Pujol, J, Ortiz, H, Lopez-Sola, M, Hernandez-Ribas, R, Deus, J, Alonso, P, Yucel, M, Pantelis, C, Menchon, JM, Cardoner, N (2009). Altered corticostriatal functional connectivity in obsessive-compulsive disorder. Archives of General Psychiatry 66, 11891200.Google Scholar
Johansen-Berg, H, Gutman, DA, Behrens, TE, Matthews, PM, Rushworth, MF, Katz, E, Lozano, AM, Mayberg, HS (2008). Anatomical connectivity of the subgenual cingulate region targeted with deep brain stimulation for treatment-resistant depression. Cerebral Cortex 18, 13741383.Google Scholar
Kaufman, J, Birmaher, B, Brent, D, Rao, U, Flynn, C, Moreci, P, Williamson, D, Ryan, N (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry 36, 980988.CrossRefGoogle ScholarPubMed
Kotov, R, Gamez, W, Schmidt, F, Watson, D (2010). Linking ‘big’ personality traits to anxiety, depressive, and substance use disorders: a meta-analysis. Psychological Bulletin 136, 768821.CrossRefGoogle ScholarPubMed
Lewinsohn, PM, Rohde, P, Seeley, JR (1998). Major depressive disorder in older adolescents: prevalence, risk factors, and clinical implications. Clinical Psychology Review 18, 765794.CrossRefGoogle ScholarPubMed
Lewinsohn, PM, Steinmetz, JL, Larson, DW, Franklin, J (1981). Depression-related cognitions: antecedent or consequence? Journal of Abnormal Psychology 90, 213219.CrossRefGoogle ScholarPubMed
Matthews, SC, Strigo, IA, Simmons, AN, Yang, TT, Paulus, MP (2008). Decreased functional coupling of the amygdala and supragenual cingulate is related to increased depression in unmedicated individuals with current major depressive disorder. Journal of Affective Disorders 111, 1320.CrossRefGoogle ScholarPubMed
Monroe, SM, Harkness, KL (2011). Recurrence in major depression: a conceptual analysis. Psychological Review 118, 655674.CrossRefGoogle ScholarPubMed
Norris, CJ, Larsen, JT, Cacioppo, JT (2007). Neuroticism is associated with larger and more prolonged electrodermal responses to emotionally evocative pictures. Psychophysiology 44, 823826.Google Scholar
Ongur, D, An, X, Price, JL (1998). Prefrontal cortical projections to the hypothalamus in macaque monkeys. Journal of Comparative Neurology 401, 480505.Google Scholar
Ongur, D, Price, JL (2000). The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cerebral Cortex 10, 206219.Google Scholar
Pezawas, L, Meyer-Lindenberg, A, Drabant, EM, Verchinski, BA, Munoz, KE, Kolachana, BS, Egan, MF, Mattay, VS, Hariri, AR, Weinberger, DR (2005). 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nature Neuroscience 8, 828834.CrossRefGoogle ScholarPubMed
Post, RM, Weiss, SR (1998). Sensitization and kindling phenomena in mood, anxiety, and obsessive-compulsive disorders: the role of serotonergic mechanisms in illness progression. Biological Psychiatry 44, 193206.CrossRefGoogle ScholarPubMed
Price, JL, Drevets, WC (2010). Neurocircuitry of mood disorders. Neuropsychopharmacology 35, 192216.Google Scholar
Putnam, SP, Ellis, LK, Rothbart, MK (2001). The structure of temperament from infancy through adolescence. In Advances in Research on Temperament (ed. Eliasz, A. and Angleitner, A.), pp. 165182. Pabst Science: Lengerich, Germany.Google Scholar
Radloff, LS (1977). The CES-D scale: a self-reported depression scale for research in the general population. Applied Psychological Measurement 1, 385401.Google Scholar
Reynaud, E, El Khoury-Malhame, M, Rossier, J, Blin, O, Khalfa, S (2012). Neuroticism modifies psychophysiological responses to fearful films. PLoS ONE 7, e32413.CrossRefGoogle ScholarPubMed
Rohde, P, Lewinsohn, PM, Seeley, JR (1994). Are adolescents changed by an episode of major depression? Journal of the American Academy of Child and Adolescent Psychiatry 33, 12891298.Google Scholar
Roy, AK, Shehzad, Z, Margulies, DS, Kelly, AM, Uddin, LQ, Gotimer, K, Biswal, BB, Castellanos, FX, Milham, MP (2009). Functional connectivity of the human amygdala using resting state fMRI. Neuroimage 45, 614626.Google Scholar
Rutter, M (1987). Temperament, personality and personality disorder. British Journal of Psychiatry 150, 443458.Google Scholar
Shea, MT, Leon, AC, Mueller, TI, Solomon, DA, Warshaw, MG, Keller, MB (1996). Does major depression result in lasting personality change? American Journal of Psychiatry 153, 14041410.Google ScholarPubMed
Shehzad, Z, Kelly, AM, Reiss, PT, Gee, DG, Gotimer, K, Uddin, LQ, Lee, SH, Margulies, DS, Roy, AK, Biswal, BB, Petkova, E, Castellanos, FX, Milham, MP (2009). The resting brain: unconstrained yet reliable. Cerebral Cortex 19, 22092229.Google Scholar
Sheline, YI, Barch, DM, Donnelly, JM, Ollinger, JM, Snyder, AZ, Mintun, MA (2001). Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biological Psychiatry 50, 651658.Google Scholar
Stein, JL, Wiedholz, LM, Bassett, DS, Weinberger, DR, Zink, CF, Mattay, VS, Meyer-Lindenberg, A (2007). A validated network of effective amygdala connectivity. Neuroimage 36, 736745.Google Scholar
Strelau, J (1982). Biologically determined dimensions of personality or temperament? Personality and Individual Differences 3, 355360.Google Scholar
Tellegen, A (1985). Structures of mood and personality and their relevance to assessing anxiety, with an emphasis on self-report. In Anxiety and the Anxiety Disorders, (ed. A. H. Tuma and J. D. Masur), pp. 681706. Lawrence Erlbaum Associates Inc.: Hillsdale, NJ.Google Scholar
van den Heuvel, MP, Hulshoff Pol, HE (2010). Exploring the brain network: a review on resting-state fMRI functional connectivity. European Neuropsychopharmacology 20, 519534.Google Scholar
Van Dijk, KR, Hedden, T, Venkataraman, A, Evans, KC, Lazar, SW, Buckner, RL (2010). Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. Journal of Neurophysiology 103, 297321.CrossRefGoogle ScholarPubMed
Van Dijk, KR, Sabuncu, MR, Buckner, RL (2012). The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 59, 431438.CrossRefGoogle ScholarPubMed
Watson, D, Clark, LA (1984). Negative affectivity: the disposition to experience aversive emotional states. Psychological Bulletin 96, 465490.CrossRefGoogle ScholarPubMed
Whittle, S, Yap, MB, Yucel, M, Fornito, A, Simmons, JG, Barrett, A, Sheeber, L, Allen, NB (2008). Prefrontal and amygdala volumes are related to adolescents’ affective behaviors during parent-adolescent interactions. Proceedings of the National Academy of Sciences USA 105, 36523657.Google Scholar
Wilson, S, Dirago, AC, Iacono, WG (2014). Prospective inter-relationships between late adolescent personality and major depressive disorder in early adulthood. Psychological Medicine 44, 567577.CrossRefGoogle ScholarPubMed
Yap, MB, Allen, NB, Ladouceur, CD (2008). Maternal socialization of positive affect: the impact of invalidation on adolescent emotion regulation and depressive symptomatology. Child Development 79, 14151431.CrossRefGoogle ScholarPubMed
Zald, DH, Mattson, DL, Pardo, JV (2002). Brain activity in ventromedial prefrontal cortex correlates with individual differences in negative affect. Proceedings of the National Academy of Sciences USA 99, 24502454.Google Scholar
Zeiss, AM, Lewinsohn, PM (1988). Enduring deficits after remissions of depression: a test of the scar hypothesis. Behaviour Research and Therapy 26, 151158.Google Scholar
Supplementary material: PDF

Davey Supplementary Material

Table S1 and Figures S1-S2

Download Davey Supplementary Material(PDF)
PDF 4.6 MB