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Dysfunction of emotional brain systems in individuals at high risk of mood disorder with depression and predictive features prior to illness

Published online by Cambridge University Press:  17 September 2014

H. C. Whalley ,
J. E. Sussmann ,
L. Romaniuk ,
T. Stewart ,
S. Kielty ,
S. M. Lawrie ,
J. Hall  and
A. M. McIntosh
H. C. Whalley*
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
J. E. Sussmann
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
L. Romaniuk
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
T. Stewart
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
S. Kielty
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
S. M. Lawrie
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
J. Hall
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK Neuroscience and Mental Health Research Institute, Cardiff University, Cardiff, UK
A. M. McIntosh
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
*
*Address for correspondence: Dr H. C. Whalley, Ph.D., University of Edinburgh, Royal Edinburgh Hospital, Morningside Park, Edinburgh EH10 5HF, UK. (Email: [email protected])
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Abstract

Background.

Abnormalities of emotion-related brain circuitry, including cortico-thalamic-limbic regions underpin core symptoms of bipolar disorder (BD) and major depressive disorder (MDD). It is unclear whether these abnormalities relate to symptoms of the disorder, are present in unaffected relatives, or whether they can predict future illness.

Method.

The Bipolar Family Study (BFS) is a prospective longitudinal study that has examined individuals at familial risk of mood disorder and healthy controls on three occasions, 2 years apart. The current study concerns imaging data from the second assessment; 51 controls and 81 high-risk (HR) individuals performing an emotional memory task. The latter group was divided into 61 HR individuals who were well, and 20 who met diagnostic criteria for MDD. At the time of the third assessment a further 11 HR individuals (from the Well group) had developed MDD. The current analyses focused on (i) differences between groups based on diagnostic status at the time of the scan, and (ii) predictors of future illness, comparing the 11 HR individuals who became unwell after the second scanning assessment to those who remained well.

Results.

All groups demonstrated typical emotional modulation of memory and associated brain activations. For analysis (i) the HR MDD group demonstrated increased thalamic activation v. HR Well. (ii) HR Well individuals who subsequently became ill showed increased activation of thalamus, insula and anterior cingulate compared to those who remained well.

Conclusions.

These findings suggest evidence for specific changes related to the presence of illness and evidence that changes in brain function in cortico-thalamic-limbic regions precede clinical illness.

Keywords

Bipolar disorderfMRIinsulamajor depressive disorderthalamus
Type
Original Articles
Information
Psychological Medicine , Volume 45 , Issue 6 , April 2015 , pp. 1207 - 1218
Copyright
Copyright © Cambridge University Press 2014 

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References

Akiskal, H, Mendlowicz, M, Jean-Louis, G, Rapaport, M, Kelsoe, J, Gillin, J, Smith, T (2005). TEMPS-A: validation of a short version of a self-rated instrument designed to measure variations in temperament. Journal of Affective Disorders 85, 45–52.CrossRefGoogle Scholar
Arnold, J, Fitzgerald, D, Fernández, G, Rijpkema, M, Rinck, M, Eling, P, Becker, E, Speckens, A, Tendolkar, I (2011). Rose or black-coloured glasses? Altered neural processing of positive events during memory formation is a trait marker of depression. Journal of Affective Disorders 131, 214–223.Google Scholar
Bair, M, Robinson, R, Katon, W, Kroenke, K (2003). Depression and pain comorbidity. Archives of Internal Medicine 163, 2433–2445.CrossRefGoogle ScholarPubMed
Bertocci, M, Bebko, G, Mullin, B, Langenecker, S, Ladouceur, C, Almeida, J, Phillips, M (2012). Abnormal anterior cingulate cortical activity during emotional n-back task performance distinguishes bipolar from unipolar depressed females. Psychological Medicine 42, 1417–1428.Google Scholar
Cahill, L, McGaugh, JL (1995). A novel demonstration of enhanced memory associated with emotional arousal. Consciousness and Cognition 4, 410–421.CrossRefGoogle ScholarPubMed
Cahill, L, McGaugh, JL (1998). Mechanisms of emotional arousal and lasting declarative memory. Trends in Neurosciences 21, 294–299.Google Scholar
Canli, T (2004). Functional brain mapping of extraversion and neuroticism: learning from individual differences in emotion processing. Journal of Personality 72, 1105–1132.Google Scholar
Canli, T, Zhao, Z, Brewer, J, Gabrieli, JD, Cahill, L (2000). Event-related activation in the human amygdala associates with later memory for individual emotional experience. The Journal of Neuroscience 20, RC99.CrossRefGoogle ScholarPubMed
Connolly, C, Wu, J, Ho, T, Hoeft, F, Wolkowitz, O, Eisendrath, S, Frank, G, Hendren, R, Max, J, Paulus, M, Tapert, S, Banerjee, D, Simmons, A, Yang, T (2013). Resting-state functional connectivity of subgenual anterior cingulate cortex in depressed adolescents. Biological Psychiatry 74, 898–907.CrossRefGoogle ScholarPubMed
Derryberry, D, Reed, MA (1994). Temperament and attention: orienting toward and away from positive and negative signals. Journal of Personality and Social Psychology 66, 1128–1139.CrossRefGoogle ScholarPubMed
Dickstein, DP, Rich, BA, Roberson-Nay, R, Berghorst, L, Vinton, D, Pine, DS, Leibenluft, E (2007). Neural activation during encoding of emotional faces in pediatric bipolar disorder. Bipolar Disorders 9, 679–692.CrossRefGoogle ScholarPubMed
Diener, C, Kuehner, C, Brusniak, W, Ubl, B, Wessa, M, Flor, H (2012). A meta-analysis of neurofunctional imaging studies of emotion and cognition in major depression. NeuroImage 61, 677–685.CrossRefGoogle ScholarPubMed
Dolcos, F, LaBar, K, Cabeza, R (2004). Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 42, 855–863.CrossRefGoogle ScholarPubMed
Duffy, A (2010). From predisposition to illness: genetically sensitive intermediate pathways to mood disorders. British Journal of Psychiatry 197, 341–342.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JB (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition with Psychotic Screen. Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
Garavan, H, Pendergrass, J, Ross, T, Stein, E, Risinger, R (2001). Amygdala response to both positively and negatively valenced stimuli. Neuroreport 12, 2779–2783.CrossRefGoogle ScholarPubMed
Green, EK, Grozeva, D, Jones, I, Jones, L, Kirov, G, Caesar, S, Gordon-Smith, K, Fraser, C, Forty, L, Russell, E, Hamshere, ML, Moskvina, V, Nikolov, I, Farmer, A, McGuffin, P, Holmans, PA, Owen, MJ, O'Donovan, MC, Craddock, N (2010). The bipolar disorder risk allele at CACNA1C also confers risk of recurrent major depression and of schizophrenia. Molecular Psychiatry 15, 1016–1022.Google Scholar
Haas, BW, Canli, T (2008). Emotional memory function, personality structure and psychopathology: a neural system approach to the identification of vulnerability markers. Brain Research Reviews 58, 71–84.Google Scholar
Hall, J, Harris, J, McKirdy, J, Johnstone, E, Lawrie, SM (2007). Emotional memory in schizophrenia. Neuropsychologia 45, 1152–1159.Google Scholar
Hamann, S, Ely, T, Grafton, S, Kilts, C (1999). Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nature Neuroscience 2, 289–293.Google Scholar
Hamann, S, Mao, H (2002). Positive and negative emotional verbal stimuli elicit activity in the left amygdala. Neuroreport 13, 15–19.Google Scholar
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 56–62.CrossRefGoogle ScholarPubMed
Hillegers, M, Reichart, C, Wals, M, Verhulst, F, Ormel, J, Nolen, W (2005). Five-year prospective outcome of psychopathology in the adolescent offspring of bipolar parents. Bipolar Disorders 7, 344–350.CrossRefGoogle ScholarPubMed
Kauer-Sant'anna, M, Yatham, LN, Tramontina, J, Weyne, F, Cereser, KM, Gazalle, FK, Andreazza, AC, Santin, A, Quevedo, J, Izquierdo, I, Kapczinski, F (2008). Emotional memory in bipolar disorder. The British Journal of Psychiatry 192, 458–463.Google Scholar
Keightley, ML, Seminowicz, DA, Bagby, RM, Costa, P, Fossati, P, Mayberg, HS (2003). Personality influences limbic-cortical interactions during sad mood induction. NeuroImage 20, 2031–2039.CrossRefGoogle ScholarPubMed
Kerestes, R, Ladouceur, C, Meda, S, Nathan, P, Blumberg, H, Maloney, K, Ruf, B, Saricicek, A, Pearlson, G, Bhagwagar, Z, Phillips, M (2012). Abnormal prefrontal activity subserving attentional control of emotion in remitted depressed patients during a working memory task with emotional distracters. Psychological Medicine 42, 29–40.Google Scholar
LaBar, KS, Cabeza, R (2006). Cognitive neuroscience of emotional memory. Nature Reviews Neuroscience 7, 54–64.CrossRefGoogle ScholarPubMed
Lang, P, Bradley, MM (2007). The International Affective Picture System (IAPS) in the Study of Emotion and Attention. Handbook of Emotion Elicitation and Assessment. Oxford University Press: Oxford, UK.Google Scholar
Liu, Y, Blackwood, DH, Caesar, S, de Geus, EJ, Farmer, A, Ferreira, MA, Ferrier, N, Fraser, C, Gordon-Smith, K, Green, EK, Grozeva, D, Gurling, HM, Hamshere, ML, Heutink, P, Holmans, PA, Hoogendijk, WJ, Hottenga, JJ, Jones, L, Jones, IR, Kirov, G, Lin, D, McGuffin, P, Moskvina, V, Nolen, WA, Perlis, RH, Posthuma, D, Scolnick, EM, Smit, AB, Smit, JH, Smoller, JW, St Clair, D, van Dyck, R, Verhage, M, Willemsen, G, Young, AH, Zandbelt, T, Boomsma, DI, Craddock, N, O'Donovan, MC, Owen, MJ, Penninx, BW, Purcell, S, Sklar, P, Sullivan, PF (2011). Meta-analysis of genome-wide association data of bipolar disorder and major depressive disorder. Molecular Psychiatry 16, 2–4.CrossRefGoogle ScholarPubMed
Lépine, J, Briley, M (2004). The epidemiology of pain in depression. Human Psychopharmacology: Clinical and Experimental 19, S3–S7.Google Scholar
Maldjian, J, Laurienti, P, Kraft, R, Burdette, J (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19, 1233–1239.Google Scholar
McCrae, R, John, O (1992). An introduction to the five-factor model and its applications. Journal of Personality 60, 175–215.Google Scholar
McGuffin, P, Farmer, A, Harvey, I (1991). A polydiagnostic application of operational criteria in studies of psychotic illness. Development and reliability of the OPCRIT system. Archives of General Psychiatry 48, 764–770.CrossRefGoogle ScholarPubMed
McGuffin, P, Rijsdijk, F, Andrew, M, Sham, P, Katz, R, Cardno, AB (2003). The heritability of bipolar affective disorder and the genetic relationship to unipolar depression. Archives of General Psychiatry 60, 497–502.CrossRefGoogle ScholarPubMed
Mutschler, I, Ball, T, Wankerl, J, Strigo, I (2012). Pain and emotion in the insular cortex: evidence for functional reorganization in major depression. Neuroscience Letters 520, 204–209.CrossRefGoogle ScholarPubMed
Phelps, EA (2004). Human emotion and memory: interactions of the amygdala and hippocampal complex. Current Opinion in Neurobiology 14, 198–202.CrossRefGoogle ScholarPubMed
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003). Neurobiology of emotion perception II: implications for major psychiatric disorders. Biological Psychiatry 54, 515–528.Google Scholar
Rock, PL, Goodwin, GM, Harmer, CJ (2010). The common adolescent bipolar phenotype shows positive biases in emotional processing. Bipolar Disorders 12, 606–615.CrossRefGoogle ScholarPubMed
Sacher, J, Neumann, J, Fünfstück, T, Soliman, A, Villringer, A, Schroeter, ML (2012). Mapping the depressed brain: a meta-analysis of structural and functional alterations in major depressive disorder. Journal of Affective Disorders 140, 142–148.Google Scholar
Savitz, J, Drevets, WC (2009). Bipolar and major depressive disorder: neuroimaging the developmental-degenerative divide. Neuroscience and Biobehavioral Reviews 33, 699–771.Google Scholar
Schulze, TG, Akula, N, Breuer, R, Steele, J, Nalls, MA, Singleton, AB, Degenhardt, FA, Nöthen, MM, Cichon, S, Rietschel, M, McMahon, FJ (2014). Molecular genetic overlap in bipolar disorder, schizophrenia, and major depressive disorder. World Journal of Biological Psychiatry 15, 200–208.Google Scholar
Strigo, IA, Matthews, SC, Simmons, AN (2013). Decreased frontal regulation during pain anticipation in unmedicated subjects with major depressive disorder. Translational Psychiatry 3, e239.CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroi, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273–289.Google Scholar
Van Wingen, GA, van Eijndhoven, P, Tendolkar, I, Buitelaar, J, Verkes, RJ, Fernández, G (2011). Neural basis of emotion recognition deficits in first-episode major depression. Psychological Medicine 41, 1397–1405.Google Scholar
Whalley, HC, McKirdy, J, Romaniuk, L, Sussmann, J, Johnstone, EC, Wan, HI, McIntosh, AM, Lawrie, SM, Hall, J (2009). Functional imaging of emotional memory in bipolar disorder and schizophrenia. Bipolar Disorders 11, 840–856.Google Scholar
Whalley, HC, Sussmann, JE, Chakirova, G, Mukerjee, P, Peel, A, McKirdy, J, Hall, J, Johnstone, EC, Lawrie, SM, McIntosh, AM (2011). The neural basis of familial risk and temperamental variation in individuals at high risk of bipolar disorder. Biological Psychiatry 70, 343–349.CrossRefGoogle ScholarPubMed
Whalley, HC, Sussmann, JE, Romaniuk, L, Stewart, T, Papmeyer, M, Sprooten, E, Hackett, S, Hall, J, Lawrie, SM, McIntosh, AM (2013). Prediction of depression in individuals at high familial risk of mood disorders using functional magnetic resonance imaging. PloS One 8, e57357.Google Scholar
Yeh, ZTT, Hua, MSS (2009). Effects of depressive disorder on false memory for emotional information. Depression and Anxiety 26, 456–463.Google Scholar
Young, K, Holcomb, L, Yazdani, U, Hicks, P, German, D (2004). Elevated neuron number in the limbic thalamus in major depression. The American Journal of Psychiatry 161, 1270–1277.Google Scholar
Young, RC, Biggs, JT, Ziegler, VE, Meyer, DA (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429–435.Google Scholar
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