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Amygdala to hippocampal volume ratio is associated with negative memory bias in healthy subjects

Published online by Cambridge University Press:  11 July 2011

L. Gerritsen*
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands Department of Psychiatry, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
M. Rijpkema
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands
I. van Oostrom
Affiliation:
Department of Psychiatry, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
J. Buitelaar
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands
B. Franke
Affiliation:
Department of Human Genetics, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
G. Fernández
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands Department of Cognitive Neuroscience, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
I. Tendolkar
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands Department of Psychiatry, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands Department of Psychiatry, Faculty of Medicine and Clinic for Psychiatry and Psychotherapy, University of Duisburg-Essen, Essen, Germany
*
*Address for correspondence: Dr L. Gerritsen, PO Box 9101, 6500 HB Nijmegen, The Netherlands. (Email: [email protected])

Abstract

Background

Negative memory bias is thought to be one of the main cognitive risk and maintenance factors for depression, but its neural substrates are largely unknown. Here, we studied whether memory bias is related to amygdala and hippocampal volume, two structures that are critical for emotional memory processes and that show consistent volume alterations in depression.

Method

Structural magnetic resonance imaging (MRI) was carried out in 272 healthy participants (62% female, 18–50 years old). All images were acquired on 1.5 T Siemens MRI scanners. Automatic segmentation of amygdala and hippocampus was performed using the FIRST module of FSL. Negative memory bias was assessed by the self-referent encoding/evaluation test.

Results

Negative memory bias was associated with larger amygdala (p=0.042) and smaller hippocampal (p=0.029) volumes. In additional analyses, we found that, compared with the associations found with hippocampus and amygdala volume separately, a stronger association was found between negative memory bias and the ratio of amygdala:hippocampus volume (p=0.021).

Conclusions

In non-depressed subjects we found that larger amygdala and smaller hippocampal volumes are associated with negative memory bias. This suggests that an increased amygdala:hippocampus volume ratio plays a role in cognitive vulnerability often seen in individuals with high risk for depression and that these structural brain differences may pre-date the onset of depression.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2011

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References

Amico, F, Meisenzahl, E, Koutsouleris, N, Reiser, M, Moller, HJ, Frodl, T (2011). Structural MRI correlates for vulnerability and resilience to major depressive disorder. Journal of Psychiatry and Neuroscience 36, 1522.CrossRefGoogle ScholarPubMed
Anand, A, Shekhar, A (2003). Brain imaging studies in mood and anxiety disorders: special emphasis on the amygdala. Annals of New York Academy of Science 985, 370388.CrossRefGoogle ScholarPubMed
Ashburner, J, Friston, KJ (2000). Voxel-based morphometry – the methods. Neuroimage 11, 805821.CrossRefGoogle ScholarPubMed
Barnes, J, Foster, J, Boyes, RG, Pepple, T, Moore, EK, Schott, JM, Frost, C, Scahill, RI, Fox, NC (2008). A comparison of methods for the automated calculation of volumes and atrophy rates in the hippocampus. Neuroimage 40, 16551671.CrossRefGoogle ScholarPubMed
Beck, AT, Rush, AJ, Shaw, BF, Emery, G (1979). Cognitive Therapy of Depression. Guilford Press: New York.Google Scholar
Bradley, B, Mogg, K, Galbraith, M, Perrett, A (1993). Negative recall bias and neuroticism: state vs trait effects. Behaviour, Research and Therapy 31, 125127.CrossRefGoogle ScholarPubMed
Bradley, BP, Mogg, K (1994). Mood and personality in recall of positive and negative information. Research and Therapy 32, 137141.CrossRefGoogle ScholarPubMed
Cahill, L, Babinsky, R, Markowitsch, HJ, McGaugh, JL (1995). The amygdala and emotional memory. Nature 377, 295296.CrossRefGoogle ScholarPubMed
Cahill, L, Gorski, L, Le, K (2003). Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding. Learning and Memory 10, 270274.CrossRefGoogle ScholarPubMed
Chen, MC, Hamilton, JP, Gotlib, IH (2010). Decreased hippocampal volume in healthy girls at risk of depression. Archives of General Psychiatry 67, 270276.CrossRefGoogle ScholarPubMed
Czeh, B, Lucassen, PJ (2007). What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated? European Archives of Psychiatry and Clinical Neuroscience 257, 250260.CrossRefGoogle ScholarPubMed
de Geus, EJ, van't Ent, D, Wolfensberger, SP, Heutink, P, Hoogendijk, WJ, Boomsma, DI, Veltman, DJ (2007). Intrapair differences in hippocampal volume in monozygotic twins discordant for the risk for anxiety and depression. Biological Psychiatry 61, 10621071.CrossRefGoogle ScholarPubMed
Dolcos, F, LaBar, KS, Cabeza, R (2005). Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. Proceedings of the National Academy of Sciences 102, 26262631.CrossRefGoogle ScholarPubMed
Drevets, WC (2003). Neuroimaging abnormalities in the amygdala in mood disorders. Annals of New York Academy of Science 985, 420444.CrossRefGoogle ScholarPubMed
Frodl, T, Meisenzahl, EM, Zetzsche, T, Born, C, Jager, M, Groll, C, Bottlender, R, Leinsinger, G, Moller, HJ (2003). Larger amygdala volumes in first depressive episode as compared to recurrent major depression and healthy control subjects. Biological Psychiatry 53, 338344.CrossRefGoogle ScholarPubMed
Frodl, T, Meisenzahl, EM, Zetzsche, T, Hohne, T, Banac, S, Schorr, C, Jager, M, Leinsinger, G, Bottlender, R, Reiser, M, Moller, HJ (2004). Hippocampal and amygdala changes in patients with major depressive disorder and healthy controls during a 1-year follow-up. Journal of Clinical Psychiatry 65, 492499.CrossRefGoogle ScholarPubMed
Frodl, TS, Koutsouleris, N, Bottlender, R, Born, C, Jager, M, Scupin, I, Reiser, M, Moller, HJ, Meisenzahl, EM (2008). Depression-related variation in brain morphology over 3 years: effects of stress? Archives of General Psychiatry 65, 11561165.CrossRefGoogle ScholarPubMed
Gerritsen, L, Tendolkar, I, Franke, B, Vasquez, AA, Kooijman, S, Buitelaar, J, Fernandez, G, Rijpkema, M (2011). BDNF Val66Met genotype modulates the effect of childhood adversity on subgenual anterior cingulate cortex volume in healthy subjects. Molecular Psychiatry. Published online 17 May 2011. doi:10.1038/mp.2011.51.Google ScholarPubMed
Gilboa, E, Roberts, JE, Gotlib, IH (1997). The effects of induced and naturally occurring dysphoric mood on biases in self-evaluation and memory. Cognition & Emotion 11, 6582.CrossRefGoogle Scholar
Gordon, E, Barnett, KJ, Cooper, NJ, Tran, N, Williams, LM (2008). An ‘integrative neuroscience’ platform: application to profiles of negativity and positivity bias. Journal of Integrative Neuroscience 7, 345366.CrossRefGoogle ScholarPubMed
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, 7184.CrossRefGoogle Scholar
Hamilton, JP, Gotlib, IH (2008). Neural substrates of increased memory sensitivity for negative stimuli in major depression. Biological Psychiatry 63, 11551162.CrossRefGoogle ScholarPubMed
Hammen, C, Zupan, BA (1984). Self-schemas, depression, and the processing of personal information in children. Journal of Experimental Child Psychology 37, 598608.CrossRefGoogle ScholarPubMed
Hasler, G, Drevets, WC, Manji, HK, Charney, DS (2004). Discovering endophenotypes for major depression. Neuropsychopharmacology 29, 17651781.CrossRefGoogle ScholarPubMed
Hayden, EP, Dougherty, LR, Maloney, B, Olino, TM, Sheikh, H, Durbin, CE, Nurnberger, JI Jr., Lahiri, DK, Klein, DN (2008). Early-emerging cognitive vulnerability to depression and the serotonin transporter promoter region polymorphism. Journal of Affective Disorders 107, 227230.CrossRefGoogle ScholarPubMed
Holzel, BK, Carmody, J, Evans, KC, Hoge, EA, Dusek, JA, Morgan, L, Pitman, RK, Lazar, SW (2010). Stress reduction correlates with structural changes in the amygdala. Social Cognitive & Affective Neuroscience 5, 1117.CrossRefGoogle ScholarPubMed
Jovicich, J, Czanner, S, Han, X, Salat, D, van der, KA, Quinn, B, Pacheco, J, Albert, M, Killiany, R, Blacker, D, Maguire, P, Rosas, D, Makris, N, Gollub, R, Dale, A, Dickerson, BC, Fischl, B (2009). MRI-derived measurements of human subcortical, ventricular and intracranial brain volumes: reliability effects of scan sessions, acquisition sequences, data analyses, scanner upgrade, scanner vendors and field strengths. Neuroimage 46, 177192.CrossRefGoogle ScholarPubMed
Kendler, KS, Fiske, A, Gardner, CO, Gatz, M (2009). Delineation of two genetic pathways to major depression. Biological Psychiatry 65, 808811.CrossRefGoogle ScholarPubMed
Kronmuller, KT, Pantel, J, Kohler, S, Victor, D, Giesel, F, Magnotta, VA, Mundt, C, Essig, M, Schroder, J (2008). Hippocampal volume and 2-year outcome in depression. British Journal of Psychiatry 192, 472473.CrossRefGoogle ScholarPubMed
LaBar, KS, Cabeza, R (2006). Cognitive neuroscience of emotional memory. Nature Reviews Neuroscience 7, 5464.CrossRefGoogle ScholarPubMed
McEwen, BS (2001). Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Annals of the New York Academy of Science 933, 265277.CrossRefGoogle ScholarPubMed
MacMillan, S, Szeszko, PR, Moore, GJ, Madden, R, Lorch, E, Ivey, J, Banerjee, SP, Rosenberg, DR (2003). Increased amygdala: hippocampal volume ratios associated with severity of anxiety in pediatric major depression. Journal of Child & Adolescence Psychopharmacology 13, 6573.CrossRefGoogle ScholarPubMed
MacQueen, G, Frodl, T (2010). The hippocampus in major depression: evidence for the convergence of the bench and bedside in psychiatric research? Molecular Psychiatry 16, 252264.CrossRefGoogle ScholarPubMed
Martin, M, Ward, JC, Clark, DM (1983). Neuroticism and the recall of positive and negative personality information. Behaviour Research and Therapy 21, 495503.CrossRefGoogle ScholarPubMed
Patenaude, B, Smith, SM, Kennedy, DN, Jenkinson, M (2011). A Bayesian model of shape and appearance for subcortical brain segmentation. NeuroImage 56, 907922.CrossRefGoogle ScholarPubMed
Phelps, EA (2004). Human emotion and memory: interactions of the amygdala and hippocampal complex. Current Opinion in Neurobiology 14, 198202.CrossRefGoogle ScholarPubMed
Ramel, W, Goldin, PR, Eyler, LT, Brown, GG, Gotlib, IH, McQuaid, JR (2007). Amygdala reactivity and mood-congruent memory in individuals at risk for depressive relapse. Biological Psychiatry 61, 231239.CrossRefGoogle ScholarPubMed
Rao, U, Chen, LA, Bidesi, AS, Shad, MU, Thomas, MA, Hammen, CL (2010). Hippocampal changes associated with early-life adversity and vulnerability to depression. Biological Psychiatry 67, 357364.CrossRefGoogle ScholarPubMed
Reips, UD (2002). Standards for Internet-based experimenting. Experimental Psychology 49, 243256.Google ScholarPubMed
Richardson, MP, Strange, BA, Dolan, RJ (2004). Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nature Neuroscience 7, 278285.CrossRefGoogle ScholarPubMed
Robinson, OJ, Cools, R, Crockett, MJ, Sahakian, BJ (2010). Mood state moderates the role of serotonin in cognitive biases. Journal of Psychopharmacology 24, 573583.CrossRefGoogle ScholarPubMed
Scoville, WB, Milner, B (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry 20, 1121.CrossRefGoogle ScholarPubMed
Sheline, YI, Gado, MH, Kraemer, HC (2003). Untreated depression and hippocampal volume loss. American Journal of Psychiatry 160, 15161518.CrossRefGoogle ScholarPubMed
Smith, S, Jenkinson, M, Woolrich, MW, Beckmann, CF, Behrens, TEJ, Johansen-Berg, H, Bannister, PR, DeLuca, M, Drobjnak, I, Flitney, D, Niazy, R, Saunders, J, Vickers, J, Zhang, Y, De Stefano, N, Brady, JM, Matthews, PW (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23, S208S219.CrossRefGoogle ScholarPubMed
Symons, CS, Johnson, BT (1997). The self-reference effect in memory: a meta-analysis. Psychological Bulletin 121, 371394.CrossRefGoogle ScholarPubMed
Teasdale, JD, Dent, J (1987). Cognitive vulnerability to depression: an investigation of two hypotheses. British Journal of Clinical Psychology 26, 113126.CrossRefGoogle ScholarPubMed
Timbremont, B, Braet, C, Bosmans, G, van Vlierberghe, L (2008). Cognitive biases in depressed and non-depressed referred youth. Clinical Psychology and Psychotherapy 15, 329339.CrossRefGoogle ScholarPubMed
van Eijndhoven, P, van Wingen, G, van Oijen, K, Rijpkema, M, Goraj, B, Jan, VR, Oude, VR, Fernandez, G, Buitelaar, J, Tendolkar, I (2009). Amygdala volume marks the acute state in the early course of depression. Biological Psychiatry 65, 812818.CrossRefGoogle Scholar
van Petten, C (2004). Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-analysis. Neuropsychologia 42, 13941413.CrossRefGoogle ScholarPubMed
Watkins, PC, Vache, K, Verney, SP, Muller, S, Mathews, A (1996). Unconscious mood-congruent memory bias in depression. Journal of Abnormal Psychology 105, 3441.CrossRefGoogle ScholarPubMed
Watson, D (1988). The vicissitudes of mood measurement: effects of varying descriptors, time frames, and response formats on measures of Positive and Negative Affect. Journal of Personality and Social Psychology 55, 128141.CrossRefGoogle ScholarPubMed
Williams, LM, Gatt, JM, Grieve, SM, Dobson-Stone, C, Paul, RH, Gordon, E, Schofield, PR (2010). COMT Val(108/158)Met polymorphism effects on emotional brain function and negativity bias. Neuroimage 53, 918925.CrossRefGoogle ScholarPubMed