Relationship between amygdala volume and emotion recognition in adolescents at ultra-high risk for psychosis

Psychiatry Research - Neuroimaging

Volumn 224, Issue 3, 2014, Pages 159-167

  Bartholomeusz, Cali F ^a   Whittle, Sarah L ^a   Pilioussis, Eleanor ^a   Allott, Kelly ^b   Rice, Simon ^b   Schäfer, Miriam R ^b,c   Pantelis, Christos ^a   Paul Amminger, G ^b,c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Affect perception; Limbic system; Magnetic resonance imaging; Mediation analyses; Prodrome; Prosody

Indexed keywords

ADOLESCENT; ADULT; AMYGDALOID NUCLEUS; ANGER; ARTICLE; BRAIN ASYMMETRY; BRAIN REGION; BRAIN SIZE; CLINICAL ARTICLE; DEPRESSION; FEAR; FEMALE; HEMISPHERE; HIGH RISK POPULATION; HUMAN; MALE; NEGATIVE SYNDROME; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; PSYCHOSIS; SADNESS; SEX DIFFERENCE; EMOTION; EUROPE; FACIAL EXPRESSION; HEMISPHERIC DOMINANCE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RECOGNITION; RISK; YOUNG ADULT;

ADOLESCENT; ADULT; AMYGDALA; EMOTIONS; EUROPE; FACIAL EXPRESSION; FEMALE; FUNCTIONAL LATERALITY; HUMANS; MALE; PSYCHOTIC DISORDERS; RECOGNITION (PSYCHOLOGY); RISK; SEX FACTORS; YOUNG ADULT;

EID: 84935419181     PISSN: 09254927     EISSN: 18727506     Source Type: Journal    
DOI: 10.1016/j.pscychresns.2014.10.005     Document Type: Article

References (81)

1. Adolphs, R., 2001. The neurobiology of social cognition. Current Opinions in Neurobiology 11, 231-239.
2. Adolphs, R., Tranel, D., 2004. Impaired judgments of sadness but not happiness following bilateral amygdala damage. Journal of Cognitive Neuroscience 16, 453-462.
3. Adolphs, R., Tranel, D., Hamann, S., Young, A.W., Calder, A.J., Phelps, E.A., Anderson, A., Lee, G.P., Damasio, A.R., 1999. Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia 37, 1111-1117.
4. Aleman, A., Kahn, R.S., 2005. Strange feelings: do amygdala abnormalities dysregulate the emotional brain in schizophrenia? Progress in Neurobiology 77, 283-298.
5. Amminger, G.P., Schäfer, M.R., Klier, C.M., Schlogelhofer, M., Mossaheb, N., Thompson, A., Bechdolf, A., Allott, K., McGorry, P.D., Nelson, B., 2012a. Facial and vocal affect perception in people at ultra-high risk of psychosis, first-episode schizophrenia and healthy controls. Early Intervention in Psychiatry 6, 450-454.
6. Amminger, G.P., Schäfer, M.R., Papageorgiou, K., Klier, C.M., Cotton, S.M., Harrigan, S.M., Mackinnon, A., McGorry, P.D., Berger, G.E., 2010. Long-chain omega-3 fatty acids for indicated prevention of psychotic disorders: a randomized, placebocontrolled trial. Archives of General Psychiatry 67, 146-154.
7. Amminger, G.P., Schäfer, M.R., Papageorgiou, K., Klier, C.M., Schlogelhofer, M., Mossaheb, N., Werneck-Rohrer, S., Nelson, B., McGorry, P.D., 2012b. Emotion recognition in individuals at clinical high-risk for schizophrenia. Schizophrenia Bulletin 38, 1030-1039.
8. Anderson, B.J., 2011. Plasticity of gray matter volume: the cellular and synaptic plasticity that underlies volumetric change. Developmental Psychobiology 53, 456-465.
9. Bechdolf, A., Wood, S.J., Nelson, B., Velakoulis, D., Yucel, M., Takahashi, T., Yung, A.R., Berk, M., Wong, M.T., Pantelis, C., McGorry, P.D., 2012. Amygdala and insula volumes prior to illness onset in bipolar disorder: a magnetic resonance imaging study. Psychiatry Research: Neuroimaging 201, 34-39.
10. Blair, R.J., Curran, H.V., 1999. Selective impairment in the recognition of anger induced by diazepam. Psychopharmacology (Berlin) 147, 335-338.
11. Cahill, L., Haier, R.J., White, N.S., Fallon, J., Kilpatrick, L., Lawrence, C., Potkin, S.G., Alkire, M.T., 2001. Sex-related difference in amygdala activity during emotionally influenced memory storage. Neurobiology of Learning and Memory 75, 1-9.
12. Castagna, F., Montemagni, C., Maria Milani, A., Rocca, G., Rocca, P., Casacchia, M., Bogetto, F., 2013. Prosody recognition and audiovisual emotion matching in schizophrenia: the contribution of cognition and psychopathology. Psychiatry Research 205, 192-198.
13. Chakirova, G., Welch, K.A., Moorhead, T.W., Stanfield, A.C., Hall, J., Skehel, P., Brown, V.J., Johnstone, E.C., Owens, D.G., Lawrie, S.M., McIntosh, A.M., 2010. Orbitofrontal morphology in people at high risk of developing schizophrenia. European Psychiatry 25, 366-372.
14. Chan, R.C., Li, H., Cheung, E.F., Gong, Q.Y., 2010. Impaired facial emotion perception in schizophrenia: a meta-analysis. Psychiatry Research 178, 381-390.
15. Costafreda, S.G., Brammer, M.J., David, A.S., Fu, C.H.Y., 2007. Review: Predictors of amygdala activation during the processing of emotional stimuli: a metaanalysis of 385 PET and fMRI studies. Brain Research Reviews 58, 57-70.
16. Edwards, J., Jackson, H.J., Pattison, P.E., 2002. Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. Clinical Psychology Review 22, 789-832.
17. Edwards, J., Pattison, P.E., Jackson, H.J., Wales, R.J., 2001. Facial affect and affective prosody recognition infirst-episode schizophrenia. Schizophrenia Research 48, 235-253.
18. Ekman, P., Friesen, W., 1976. Pictures of Facial Affect. Consulting Psychologists Press, PaIo Alto, CA.
19. Endicott, J., Andreasen, N., Spitzer, R.L., 1978. Family History Research Diagnostic Criteria. Biometrics Research, New York State Psychiatric Institute, New York, NY.
20. Eritaia, J., Wood, S.J., Stuart, G.W., Bridle, N., Dudgeon, P., Maruff, P., Velakoulis, D., Pantelis, C., 2000. An optimized method for estimating intracranial volume from magnetic resonance images. Magnetic Resonance in Medicine 44, 973-977.
21. Erol, A., Putgul, G., Kosger, F., Ersoy, B., 2013. Facial emotion recognition in schizophrenia: the impact of gender. Psychiatry Investigation 10, 69-74.
22. Feinberg, T.E., Rifkin, A., Schaffer, C., Walker, E., 1986. Facial discrimination and emotional recognition in schizophrenia and affective disorders. Archives of General Psychiatry 43, 276-279.
23. Fett, A.-K.J., Viechtbauer, W., Dominguez, M.-d.-G., Penn, D.L., van Os, J., Krabbendam, L., 2011. Review: the relationship between neurocognition and social cognition with functional outcomes in schizophrenia: a meta-analysis. Neuroscience and Biobehavioral Reviews 35, 573-588.
24. Fett, A.K., Maat, A., 2013. Social cognitive impairments and psychotic symptoms: what is the nature of their association? Schizophrenia Bulletin 39, 77-85.
25. Frazier, J.A., Hodge, S.M., Breeze, J.L., Giuliano, A.J., Terry, J.E., Moore, C.M., Kennedy, D.N., Lopez-Larson, M.P., Caviness, V.S., Seidman, L.J., Zablotsky, B., Makris, N., 2008. Diagnostic and sex effects on limbic volumes in early-onset bipolar disorder and schizophrenia. Schizophrenia Bulletin 34, 37-46.
26. Gee, D.G., Karlsgodt, K.H., van Erp, T.G., Bearden, C.E., Lieberman, M.D., Belger, A., Perkins, D.O., Olvet, D.M., Cornblatt, B.A., Constable, T., Woods, S.W., Addington, J., Cadenhead, K.S., McGlashan, T.H., Seidman, L.J., Tsuang, M.T., Walker, E.F., Cannon, T.D., 2012. Altered age-related trajectories of amygdala-prefrontal circuitry in adolescents at clinical high risk for psychosis: a preliminary study. Schizophrenia Research 134, 1-9.
27. Gibbs, A.A., Dazzan, P., Morgan, K.D., Naudts, K.H., Morgan, C., Hutchinson, G., Fearon, P., Leff, J., Murray, R.M., David, A.S., 2008. Sexually dimorphic changes in the amygdala in relation to delusional beliefs infirst episode psychosis. Journal of Psychiatric Research 42, 913-919.
28. Gosselin, N., Peretz, I., Johnsen, E., Adolphs, R., 2006. Amygdala damage impairs emotion recognition from music. Neuropsychologia 45, 236-244.
29. Green, M.F., Bearden, C.E., Cannon, T.D., Fiske, A.P., Hellemann, G.S., Horan, W.P., Kee, K., Kern, R.S., Lee, J., Sergi, M.J., Subotnik, K.L., Sugar, C.A., Ventura, J., Yee, C.M., Nuechterlein, K.H., 2012. Social cognition in schizophrenia, part 1: performance across phase of illness. Schizophrenia Bulletin 38, 854-864.
30. Gur, R.E., Kohler, C., Turetsky, B.I., Siegel, S.J., Kanes, S.J., Bilker, W.B., Brennan, A.R., Gur, R.C., 2004. A sexually dimorphic ratio of orbitofrontal to amygdala volume is altered in schizophrenia. Biological Psychiatry 55, 512-517.
31. Harvey, G.T., Hughes, J., McKeith, I.G., Briel, R., Ballard, C., Gholkar, A., Scheltens, P., Perry, R.H., Ince, P., O'Brien, J.T., 1999. Magnetic resonance imaging differences between dementia with Lewy bodies and Alzheimer's disease: a pilot study. Psychological Medicine 29, 181-187.
32. Hayes, A.F., 2009. Beyond Baron and Kenny: statistical mediation analysis in the new millennium. Communication Monographs 76, 408-420.
33. Hoekert, M., Kahn, R.S., Pijnenborg, M., Aleman, A., 2007. Impaired recognition and expression of emotional prosody in schizophrenia: review and meta-analysis. Schizophrenia Research 96, 135-145.
34. Jäkälä, P., Hänninen, T., Ryynänen, M., Laakso, M., Partanen, K., Mannermaa, A., Soininen, H., 1997. Fragile-X: neuropsychological test performance, CGG triplet repeat lengths, and hippocampal volumes. Journal of Clinical Investigation 100, 331-338.
35. Jenkinson, M., Smith, S., 2000. Optimization in Robust Linear Registration of Brain Images (No. TR00MJ2). Oxford Center for Functional Magnetic Resonance Imaging of the Brain, Oxford, UK.
36. Jones, S.H., Thornicroft, G., Coffey, M., Dunn, G., 1995. A brief mental health outcome scale-reliability and validity of the Global Assessment of Functioning (GAF). British Journal of Psychiatry 166, 654-659.
37. Joyal, C.C., Laakso, M.P., Tiihonen, J., Syvalahti, E., Vilkman, H., Laakso, A., Alakare, B., Rakkolainen, V., Salokangas, R.K., Hietala, J., 2003. The amygdala and schizophrenia: a volumetric magnetic resonance imaging study in first-episode, neuroleptic-naive patients. Biological Psychiatry 54, 1302-1304.
38. Kapur, S., Mizrahi, R., Li, M., 2005. From dopamine to salience to psychosis-linking biology, pharmacology and phenomenology of psychosis. Schizophrenia Research 79, 59-68.
39. Kasai, K., Shenton, M.E., Salisbury, D.F., Onitsuka, T., Toner, S.K., Yurgelun-Todd, D., Kikinis, R., Jolesz, F.A., McCarley, R.W., 2003. Differences and similarities in insular and temporal pole MRI gray matter volume abnormalities in firstepisode schizophrenia and affective psychosis. Archives of General Psychiatry 60, 1069-1077.
40. Kay, S., Fiszbein, A., Opler, L., 1987. The Positive and Negative Syndrome Scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261-276.
41. Laakso, M.P., Soininen, H., Partanen, K., Lehtovirta, M., Hallikainen, M., Hanninen, T., Helkala, E.L., Vainio, P., Riekkinen Sr, P.J., 1998. MRI of the hippocampus in Alzheimer's disease: sensitivity, specificity, and analysis of the incorrectly classified subjects. Neurobiology of Aging 19, 23-31.
42. Laviolette, S.R., 2007. Dopamine modulation of emotional processing in cortical and subcortical neural circuits: evidence for a final common pathway in schizophrenia? Schizophrenia Bulletin 33, 971-981.
43. Lavoie, S., Bartholomeusz, C.F., Nelson, B., Lin, A., McGorry, P., Velakoulis, D., Whittle, S., Yung, A., Pantelis, C., Wood, S.J., 2014. Sulcogyral pattern and sulcal count of the orbitofrontal cortex in individuals at ultra high risk for psychosis. Schizophreia Research 154, 93-99.
44. Marwick, K., Hall, J., 2008. Social cognition in schizophrenia: a review of face processing. British Medical Bulletin 88, 43-58.
45. McClure, E.B., 2000. A meta-analytic review of sex differences in facial expression processing and their development in infants, children, and adolescents. Psychological Bulletin 126, 424-453.
46. McDonald, B., Highley, J.R., Walker, M.A., Herron, B.M., Cooper, S.J., Esiri, M.M., Crow, T.J., 2000. Anomalous asymmetry of fusiform and parahippocampal gyrus gray matter in schizophrenia: a postmortem study. American Journal of Psychiatry 157, 40-47.
47. Miettinen, P.S., Pihlajamaki, M., Jauhiainen, A.M., Niskanen, E., Hanninen, T., Vanninen, R., Soininen, H., 2011. Structure and function of medial temporal and posteromedial cortices in early Alzheimer's disease. European Journal of Neuroscience 34, 320-330.
48. Montgomery, S.A., Åsberg, M., 1979. A new depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382-389.
49. Morey, R.A., Petty, C.M., Xu, Y., Hayes, J.P., Wagner, H.R., Lewis, D.V., LaBar, K.S., Styner, M., McCarthy, G., 2009. A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes. Neuroimage 45, 855-866.
50. Morrison, A.P., French, P., Walford, L., Lewis, S.W., Kilcommons, A., Green, J., Parker, S., Bentall, R.P., 2004. Cognitive therapy for the prevention of psychosis in people at ultra-high risk: randomised controlled trial. British Journal of Psychiatry 185, 291-297.
51. Myles-Worsley, M., Weaver, S., Blailes, F., 2007. Comorbid depressive symptoms in the developmental course of adolescent-onset psychosis. Early Intervention in Psychiatry 1, 183-190.
52. Nacewicz, B.M., Dalton, K.M., Johnstone, T., Long, M.T., McAuliff, E.M., Oakes, T.R., Alexander, A.L., Davidson, R.J., 2006. Amygdala volume and nonverbal social impairment in adolescent and adult males with autism. Archives of General Psychiatry 63, 1417-1428.
53. Namiki, C., Hirao, K., Yamada, M., Hanakawa, T., Fukuyama, H., Hayashi, T., Murai, T., 2007. Impaired facial emotion recognition and reduced amygdalar volume in schizophrenia. Psychiatry Research: Neuroimaging 156, 23-32.
54. Niu, L., Matsui, M., Zhou, S.Y., Hagino, H., Takahashi, T., Yoneyama, E., Kawasaki, Y., Suzuki, M., Seto, H., Ono, T., Kurachi, M., 2004. Volume reduction of the amygdala in patients with schizophrenia: a magnetic resonance imaging study. Psychiatry Research: Neuroimaging 132, 41-51.
55. Oswald, W.D., Roth, E., 1987. Der Zahlen-Verbindungs-Test (ZVT) [The number combination test]. Hogrefe, Göttingen, Germany.
56. Phelps, E.A., O'Connor, K.J., Gatenby, J.C., Gore, J.C., Grillon, C., Davis, M., 2001. Activation of the left amygdala to a cognitive representation of fear. Nature Neuroscience 4, 437-441.
57. Preacher, K.J., Hayes, A.F., 2004. SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behaviour Research Methods, Instruments and Computers 36, 717-731.
58. Rammsayer, T.H., Stahl, J., 2007. Identification of sensorimotor components accounting for individual variability in Zahlen-Verbindungs-Test (ZVT) performance. Intelligence 35, 623-630.
59. Rietdijk, J., Ising, H.K., Dragt, S., Klaassen, R., Nieman, D., Wunderink, L., Cuijpers, P., Linszen, D., van der Gaag, M., 2013. Depression and social anxiety in helpseeking patients with an ultra-high risk for developing psychosis. Psychiatry Research 209, 309-313.
60. Roberts, C., Kinsella, G., Wales, R., 1981. Disturbances in processing prosodic features of language following right hemisphere lesions. Bulletin of Postgraduate Communication, 172-183.
61. Rothman, K.J., Greenland, S., Lash, T., 2008. Modern Epidemiology, Third Edition Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia.
62. Scholten, M.R., Aleman, A., Montagne, B., Kahn, R.S., 2005. Schizophrenia and processing of facial emotions: sex matters. Schizophrenia Research 78, 61-67.
63. Stevens, J.S., Hamann, S., 2012. Sex differences in brain activation to emotional stimuli: a meta-analysis of neuroimaging studies. Neuropsychologia 50, 1578-1593.
64. Thompson, A., Papas, A., Bartholomeusz, C., Allott, K., Amminger, G.P., Nelson, B., Wood, S., Yung, A., 2012. Social cognition in clinical"at risk"for psychosis and first episode psychosis populations. Schizophrenia Research 141, 204-209.
65. Thompson, A.D., Bartholomeusz, C., Yung, A.R., 2011. Social cognition deficits and the 'ultra high risk' for psychosis population: a review of literature. Early Intervention in Psychiatry 5, 192-202.
66. Toga, A.W., Thompson, P.M., 2003. Mapping brain asymmetry. Nature Reviews Neuroscience 4, 37-48.
67. Tseng, H.H., Chen, S.H., Liu, C.M., Howes, O., Huang, Y.L., Hsieh, M.H., Liu, C.C., Shan, J.C., Lin, Y.T., Hwu, H.G., 2013. Facial and prosodic emotion recognition deficits associate with specific clusters of psychotic symptoms in schizophrenia. PLoS One 8, e66571.
68. van Winkel, R., van Nierop, M., Myin-Germeys, I., van Os, J., 2013. Childhood trauma as a cause of psychosis: linking genes, psychology, and biology. Canadian Journal of Psychiatry 58, 44-51.
69. Van't Wout, M., van Dijke, A., Aleman, A., Kessels, R.P., Pijpers, W., Kahn, R.S., 2007. Fearful faces in schizophrenia: the relationship between patient characteristics and facial affect recognition. Journal of Nervous and Mental Disease 195, 758-764.
70. Vassilopoulou, K., Papathanasiou, M., Michopoulos, I., Boufidou, F., Oulis, P., Kelekis, N., Rizos, E., Nikolaou, C., Pantelis, C., Velakoulis, D., Lykouras, L., 2013. A magnetic resonance imaging study of hippocampal, amygdala and subgenual prefrontal cortex volumes in major depression subtypes: melancholic versus psychotic depression. Journal of Affective Disorders 146, 197-204.
71. Velakoulis, D., Wood, S.J., Wong, M.T., McGorry, P.D., Yung, A., Phillips, L., Smith, D., Brewer, W., Proffitt, T., Desmond, P., Pantelis, C., 2006. Hippocampal and amygdala volumes according to psychosis stage and diagnosis: a magnetic resonance imaging study of chronic schizophrenia, first-episode psychosis, and ultra-high-risk individuals. Archives of General Psychiatry 63, 139-149.
72. Watson, C., Andermann, F., Gloor, P., Jonesgotman, M., Peters, T., Evans, A., Olivier, A., Melanson, D., Leroux, G., 1992. Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic-resonance-imaging. Neurology 42, 1743-1750.
73. Welch, K.A., Stanfield, A.C., Moorhead, T.W., Haga, K., Owens, D.C., Lawrie, S.M., Johnstone, E.C., 2010. Amygdala volume in a population with special educational needs at high risk of schizophrenia. Psychological Medicine 40, 945-954.
74. West, A.R., Grace, A.A., 2001. The role of frontal-subcortical circuits in the pathophysiology of schizophrenia. In: Lichter, D.G., Cumming, J.L. (Eds.), Frontal Subcortical Circuits in Psychiatric and Neurological Disorders. The Guilford Press, New York, pp. 372-399.
75. Whittle, S., Lichter, R., Dennison, M., Vijayakumar, N., Schwartz, O., Byrne, M., Simmons, J., Yucel, M., Pantelis, C., McGorry, P., Allen, N.B., 2014. Structural brain development and depression onset during adolescence: a longitudinal, prospective study. American Journal of Psychiatry 171 (5), 564-571.
76. Whittle, S., Yucel, M., Fornito, A., Barrett, A., Wood, S.J., Lubman, D.I., Simmons, J., Pantelis, C., Allen, N.B., 2008. Neuroanatomical correlates of temperament in early adolescents. Journal of the American Academy of Child and Adolescent Psychiatry 47, 682-693.
77. Williams, L.M., Mathersul, D., Palmer, D.M., Gur, R.C., Gur, R.E., Gordon, E., 2009. Explicit identification and implicit recognition of facial emotions: I. Age effects in males and females across 10 decades. Journal of Clinical and Experimental Neuropsychology 31, 257-277.
78. Wiltink, S., Velthorst, E., Nelson, B., McGorry, P.M., Yung, A.R., 2013. Declining transition rates to psychosis: the contribution of potential changes in referral pathways to an ultra-high-risk service. Early Intervention in Psychiatry, 14. electronic publicationhttp://dx.doi.org/10.1111/eip.12105(November).
79. Witthaus, H., Mendes, U., Brune, M., Ozgurdal, S., Bohner, G., Gudlowski, Y., Kalus, P., Andreasen, N., Heinz, A., Klingebiel, R., Juckel, G., 2010. Hippocampal subdivision and amygdalar volumes in patients in an at-risk mental state for schizophrenia. Journal of Psychiatry and Neuroscience 35, 33-40.
80. Yucel, M., Stuart, G.W., Maruff, P., Wood, S.J., Savage, G.R., Smith, D.J., Crowe, S.F., Copolov, D.L., Velakoulis, D., Pantelis, C., 2002. Paracingulate morphologic differences in males with established schizophrenia: a magnetic resonance imaging morphometric study. Biological Psychiatry 52, 15-23.
81. Yung, A., Phillips, L.J., McGorry, P.D., McFarlane, C.A., Francey, S., Harrigan, S., Patton, G.C., Jackson, H.J., 1998. Prediction of psychosis: a step towards indicated prevention of schizophrenia. British Journal of Psychiatry Supplement 172, 14-20.