Neuroanatomical correlates of genetic risk for bipolar disorder: A voxel-based morphometry study in bipolar type I patients and healthy first degree relatives

Journal of Affective Disorders

Volumn 186, Issue , 2015, Pages 110-118

  Sariçiçek, Aybala ^a,b   Yalin, Nefize ^b   Hidiroʇlu, Ceren ^b   Çavuşoʇlu, Berrin ^b   Taş, Cumhur ^c   Ceylan, Deniz ^b,d   Zorlu, Nabi ^a   Ada, Emel ^b   Tunca, Zeliha ^b   Özerdem, Ayşegül ^b  

^a IZMIR KATIP CELEBI UNIVERSITY   (Turkey)

^b DOKUZ EYLUL UNIVERSITY   (Turkey)

^c USKUDAR UNIVERSITY   (Turkey)

^d Psychiatry Clinic Gümü hane State Hospital   (Turkey)

Author keywords

Bipolar disorder; Cerebellum; Endophenotype; Inferior frontal gyrus; Voxel based morphometry

Indexed keywords

ADULT; ARTICLE; BIPOLAR I DISORDER; BRAIN ANALYSIS; BRAIN REGION; BRAIN SIZE; CEREBELLUM; CLINICAL ARTICLE; CONTROL GROUP; CONTROLLED STUDY; DATA ANALYSIS SOFTWARE; FEMALE; FIRST DEGREE RELATIVE; GENETIC PREDISPOSITION; GENETIC RISK; GRAY MATTER; HUMAN; INFERIOR FRONTAL GYRUS; LINGUAL GYRUS; LONGITUDINAL STUDY; MALE; NEUROANATOMY; NUCLEAR MAGNETIC RESONANCE IMAGING; PARAHIPPOCAMPAL GYRUS; POSTERIOR CINGULATE; PRIORITY JOURNAL; PROGNOSIS; SAMPLE SIZE; STUDENT T TEST; SUPRAMARGINAL GYRUS; VOXEL BASED MORPHOMETRY; ADOLESCENT; AGED; BIPOLAR DISORDER; BRAIN; CASE CONTROL STUDY; CROSS-SECTIONAL STUDY; ENDOPHENOTYPE; FAMILY; FAMILY HEALTH; GENETICS; MIDDLE AGED; NEUROIMAGING; PATHOLOGY; RISK FACTOR; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; BIPOLAR DISORDER; BRAIN; CASE-CONTROL STUDIES; CROSS-SECTIONAL STUDIES; ENDOPHENOTYPES; FAMILY; FAMILY HEALTH; FEMALE; GRAY MATTER; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROIMAGING; RISK FACTORS; YOUNG ADULT;

EID: 84938220863     PISSN: 01650327     EISSN: 15732517     Source Type: Journal    
DOI: 10.1016/j.jad.2015.06.055     Document Type: Article

References (86)

1. C.M. Adler, A.D. Levine, M.P. DelBello, and S.M. Strakowski Changes in gray matter volume in patients with bipolar disorder Biol. Psychiatry 58 2005 151 157
2. C.M. Adler, M.P. DelBello, K. Jarvis, A. Levine, J. Adams, and S.M. Strakowski Voxel-based study of structural changes in first-episode patients with bipolar disorder Biol. Psychiatry 61 2007 776 781
3. A. Akdemir, M.H. Türkçapar, S.D. Örsel, N. Demirergi, I. Dag, and M.H. Özbay Reliability and validity of the Turkish version of the Hamilton depression rating scale Compr. Psychiatry 42 2001 161 165
4. J.R.C. Almeida, D. Akkal, S. Hassel, M.J. Travis, L. Banihashemi, N. Kerr, D.J. Kupfer, and M.L. Phillips Reduced gray matter volume in ventral prefrontal cortex but not amygdala in bipolar disorder: significant effects of gender and trait anxiety Psychiatry Res. Neuroimaging 171 2009 54 68
5. E.M. Aminoff, K. Kveraga, and M. Bar The role of the parahippocampal cortex in cognition Trends Cogn. Sci. 17 8 2013 379 390
6. D. Arnone, J. Cavanagh, D. Gerber, S.M. Lawrie, K.P. Ebmeier, and A.M. McIntosh Magnetic resonance imaging studies in bipolar disorder and schizophrenia: meta-analysis Br. J. Psychiatry 195 2009 194 201 10.1192/bjp.bp.108.059717
7. A.R. Aron, T.W. Robbins, and R.A. Poldrack Inhibition and the right inferior frontal cortex: one decade on Trends Cogn. Sci. 18 2014 177 185
8. A.R. Aron, P.C. Fletcher, E.T. Bullmore, B.J. Sahakian, and T.W. Robbins Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans Nat. Neurosci. 6 2003 115 116
9. J. Ashburner A fast diffeomorphic image registration algorithm Neuroimage 38 2007 95 113
10. M. Atmaca, H. Ozdemir, S. Cetinkaya, S. Parmaksiz, H. Belli, A. Kursad Poyraz, E. Tezcan, and E. Ogur Cingulate gyrus volumetry in drug free bipolar patients and patients treated with valproate or valproate and quetiapine J. Psychiatr. Res. 41 2007 821 827
11. L. Baldaçara, F. Nery-Fernandes, M. Rocha, L.C. Quarantini, G.G.L. Rocha, J.L. Guimarães, C. Araújo, I. Oliveira, A. Miranda-Scippa, and A. Jackowski Is cerebellar volume related to bipolar disorder? J. Affect. Disord. 135 2011 305 309
12. C.E. Bearden, P.M. Thompson, M. Dalwani, K.M. Hayashi, A.D. Lee, M. Nicoletti, M. Trakhtenbroit, D.C. Glahn, P. Brambilla, R.B. Sassi, A.G. Mallinger, E. Frank, D.J. Kupfer, and J.C. Soares Greater cortical gray matter density in lithium-treated patients with bipolar disorder Biol. Psychiatry 62 2007 7 16
13. J. Biederman, N. Makris, E.M. Valera, M.C. Monuteaux, J.M. Goldstein, S. Buka, D.L. Boriel, S. Bandyopadhyay, D.N. Kennedy, V.S. Caviness, G. Bush, M. Aleardi, P. Hammerness, S.V. Faraone, and L.J. Seidman Towards further understanding of the co-morbidity between attention deficit hyperactivity disorder and bipolar disorder: a MRI study of brain volumes Psychol. Med. 38 2008 1045 1056
14. G.J. Blatt, D.N. Pandya, and D.L. Rosene Parcellation of cortical afferents to three distinct sectors in the parahippocampal gyrus of the rhesus monkey: an anatomical and neurophysiological study J. Comp. Neurol. 466 2003 161 179
15. E. Bora, M. Yucel, and C. Pantelis Cognitive endophenotypes of bipolar disorder: a meta-analysis of neuropsychological deficits in euthymic patients and their first-degree relatives J. Affect. Disord. 113 2009 1 20
16. E. Bora, A. Fornito, M. Yücel, and C. Pantelis Voxelwise meta-analysis of gray matter abnormalities in bipolar disorder Biol. Psychiatry 67 2010 1097 1105
17. P. Brambilla, K. Harenski, M. Nicoletti, A.G. Mallinger, E. Frank, D.J. Kupfer, M.S. Keshavan, and J.C. Soares MRI study of posterior fossa structures and brain ventricles in bipolar patients J. Psychiatr. Res. 35 2001 313 322
18. P. Brambilla, M.A. Nicoletti, K. Harenski, R.B. Sassi, A.G. Mallinger, E. Frank, D.J. Kupfer, M.S. Keshavan, and J.C. Soares Anatomical MRI study of subgenual prefrontal cortex in bipolar and unipolar subjects Neuropsychopharmacology 27 2002 792 799
19. M. Brett, I.S. Johnsrude, and A.M. Owen The problem of functional localization in the human brain Nat. Rev. Neurosci. 3 2002 243 249
20. S. Caspers, A. Schleicher, M. Bacha-Trams, N. Palomero-Gallagher, K. Amunts, and K. Zilles Organization of the human inferior parietal lobule based on receptor architectonics Cereb. Cortex 23 2013 615 628
21. S. Caspers, S.B. Eickhoff, T. Rick, A. von Kapri, T. Kuhlen, R. Huang, N.J. Shah, and K. Zilles Probabilistic fibre tract analysis of cytoarchitectonically defined human inferior parietal lobule areas reveals similarities to macaques Neuroimage 58 2011 362 380
22. X. Chen, W. Wen, G.S. Malhi, B. Ivanovski, and P.S. Sachdev Regional gray matter changes in bipolar disorder: a voxel-based morphometric study Aust. N.Z. J. Psychiatry 41 2007 327 336
23. S. Chiu, F. Widjaja, M.E. Bates, G.T. Voelbel, G. Pandina, J. Marble, J.A. Blank, J. Day, N. Brule, and R.L. Hendren Anterior cingulate volume in pediatric bipolar disorder and autism J. Affect. Disord. 105 2008 93 99
24. S. Cho, A.W.S. Metcalfe, C.B. Young, S. Ryali, D.C. Geary, and V. Menon Hippocampal-prefrontal engagement and dynamic causal interactions in the maturation of children's fact retrieval J. Cogn. Neurosci. 24 2012 1849 1866
25. L. Davachi, J.P. Mitchell, and A.D. Wagner Multiple routes to memory: distinct medial temporal lobe processes build item and source memories Proc. Natl. Acad. Sci. USA 100 2003 2157 2162
26. M.P. DelBello, S.M. Strakowski, M.E. Zimmerman, J.M. Hawkins, and K.W. Sax MRI analysis of the cerebellum in bipolar disorder: a pilot study Neuropsychopharmacology 21 1999 63 68
27. R.A. Diana, A.P. Yonelinas, and C. Ranganath Medial temporal lobe activity during source retrieval reflects information type, not memory strength J. Cogn. Neurosci. 22 2010 1808 1818
28. C. Eker, F. Simsek, E.E. YIlmazer, O. Kitis, C. Cinar, O.D. Eker, K. Coburn, and A.S. Gonul Brain regions associated with risk and resistance for bipolar I disorder: a voxel-based MRI study of patients with bipolar disorder and their healthy siblings Bipolar Disord. 16 2014 249 261
29. M.B. First, R.L. Spitzer, M. Gibbon, and J.B.W. Williams Structured Clinical Interview for DSM-IV Axis I Disorders (SCID-I), Clinical Version 1997 American Psychiatric Press Washington D.C. and London
30. S. Frangou Brain structural and functional correlates of resilience to bipolar disorder Front. Hum. Neurosci. 5 2012 184
31. J.A. Frazier, J.L. Breeze, N. Makris, A.S. Giuliano, M.R. Herbert, L. Seidman, J. Biederman, S.M. Hodge, M.E. Dieterich, E.D. Gerstein, D.N. Kennedy, S.L. Rauch, B.M. Cohen, and V.S. Caviness Cortical gray matter differences identified by structural magnetic resonance imaging in pediatric bipolar disorder Bipolar Disord. 7 2005 555 569
32. N. Gogtay, A. Ordonez, D.H. Herman, K.M. Hayashi, D. Greenstein, C. Vaituzis, M. Lenane, L. Clasen, W. Sharp, J.N. Giedd, D. Jung, T.F. Nugent Iii, A.W. Toga, E. Leibenluft, P.M. Thompson, and J.L. Rapoport Dynamic mapping of cortical development before and after the onset of pediatric bipolar illness J. Child Psychol. Psychiatry Allied Discipl. 48 2007 852 862
33. N. Gosselin, S. Samson, R. Adolphs, M. Noulhiane, M. Roy, D. Hasboun, M. Baulac, and I. Peretz Emotional responses to unpleasant music correlates with damage to the parahippocampal cortex Brain 129 2006 2585 2592
34. A. Grecucci, C. Giorgetta, N. Bonini, and A.G. Sanfey Reappraising social emotions: the role of inferior frontal gyrus, temporo-parietal junction and insula in interpersonal emotion regulation Front. Hum. Neurosci. 7 2013 523
35. T.H. Ha, K. Ha, J.H. Kim, and J.E. Choi Regional brain gray matter abnormalities in patients with bipolar II disorder: a comparison study with bipolar I patients and healthy controls Neurosci. Lett. 456 2009 44 48
36. D.M. Hafeman, G. Bebko, M.A. Bertocci, and et al. Abnormal deactivation of the inferior frontal gyrus during implicit emotion processing in youth with bipolar disorder: attenuated by medication J. Psychiatr. Res. 58 2014 129 136
37. T. Hajek, J. Cullis, T. Novak, M. Kopecek, R. Blagdon, L. Propper, P. Stopkova, A. Duffy, C. Hoschl, R. Uher, T. Paus, L.T. Young, and M. Alda Brain structural signature of familial predisposition for bipolar disorder: replicable evidence for involvement of the right inferior frontal gyrus Biol. Psychiatry 73 2013 144 152
38. T. Hajek, M. Alda, E. Hajek, and J. Ivanoff Functional neuroanatomy of response inhibition in bipolar disorders - combined voxel based and cognitive performance meta-analysis J. Psychiatr. Res 47 2013 1955 1966
39. M. Haldane, G. Cunningham, C. Androutsos, and S. Frangou Structural brain correlates of response inhibition in bipolar disorder I J. Psychopharmacol. 22 2008 138 143
40. J. Houenou, J. Frommberger, S. Carde, M. Glasbrenner, C. Diener, M. Leboyer, and M. Wessa Neuroimaging-based markers of bipolar disorder: evidence from two meta-analyses J. Affect. Disord. 132 2011 344 355
41. N. Isenberg, D. Silbersweig, A. Engelien, S. Emmerich, K. Malavade, B. Beattie, A.C. Leon, and E. Stern Linguistic threat activates the human amygdala Proc. Natl. Acad. Sci. USA 96 1999 10456 10459
42. A. Javadapour, G.S. Malhi, B. Ivanovski, X. Chen, W. Wen, and P. Sachdev Increased anterior cingulate cortex volume in bipolar I disorder Aust. N.Z. J. Psychiatry 41 2007 910 916
43. F. Karadaʇ, T. Oral, F.A. Yalçin, and E. Erten Reliability and validity of Turkish translation of Young mania rating scale Turk. Psikiyatri Derg. 13 2002 107 114
44. S. Kaur, R.B. Sassi, D. Axelson, M. Nicoletti, P. Brambilla, E.S. Monkul, J.P. Hatch, M.S. Keshavan, N. Ryan, B. Birmaher, and J.C. Soares Cingulate cortex anatomical abnormalities in children and adolescents with bipolar disorder Am. J. Psychiatry 162 2005 1637 1643
45. M.J. Kempton, M. Haldane, J. Jogia, P.M. Grasby, D. Collier, and S. Frangou Dissociable brain structural changes associated with predisposition, resilience, and disease expression in bipolar disorder J. Neurosci. 29 2009 10863 10868
46. K. Kodama, T. Terao, K. Hatano, K. Kohno, M. Makino, and Y. Mizokami Identification of the neural correlates of cyclothymic temperament using a working memory task in fMRI J. Affect. Disord. 171 2015 1 5
47. C.D. Ladouceur, J.R.C. Almeida, B. Birmaher, D.A. Axelson, S. Nau, C. Kalas, K. Monk, D.J. Kupfer, and M.L. Phillips Subcortical gray matter volume abnormalities in healthy bipolar offspring: potential neuroanatomical risk marker for bipolar disorder? J. Am. Acad. Child Adolesc. Psychiatry 47 2008 532 539
48. J.L. Lancaster, M.G. Woldorff, L.M. Parsons, M. Liotti, C.S. Freitas, L. Rainey, P.V. Kochunov, D. Nickerson, S.A. Mikiten, and P.T. Fox Automated Talairach atlas labels for functional brain mapping Hum. Brain Mapp. 10 2000 120 131
49. M. Li, L. Cui, W. Deng, X. Ma, C. Huang, L. Jiang, Y. Wang, D.A. Collier, Q. Gong, and T. Li Voxel-based morphometric analysis on the volume of gray matter in bipolar I disorder Psychiatry Res. 191 2011 92 97
50. P. Lichtenstein, B.H. Yip, C. Björk, Y. Pawitan, T.D. Cannon, P.F. Sullivan, and C.M. Hultman Common genetic determinants of schizophrenia and bipolar disorder in Swedish families: a population-based study Lancet 373 2009 234 239
51. R.A. Lochhead, R.V. Parsey, M.A. Oquendo, and J.J. Mann Regional brain gray matter volume differences in patients with bipolar disorder as assessed by optimized voxel-based morphometry Biol. Psychiatry 55 2004 1154 1162
52. I.K. Lyoo, S.R. Dager, J.E. Kim, S.J. Yoon, S.D. Friedman, D.L. Dunner, and P.F. Renshaw Lithium-induced gray matter volume increase as a neural correlate of treatment response in bipolar disorder: a longitudinal brain imaging study Neuropsychopharmacology 35 2010 1743 1750
53. I.K. Lyoo, M.J. Kim, A.L. Stoll, C.M. Demopulos, A.M. Parow, S.R. Dager, S.D. Friedman, D.L. Dunner, and P.F. Renshaw Frontal lobe gray matter density decreases in bipolar I disorder Biol. Psychiatry 55 2004 648 651 10.1016/j.biopsych.2003.10.017
54. J.A. Maldjian, P.J. Laurienti, R.A. Kraft, and J.H. Burdette An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets Neuroimage 19 2003 1233 1239
55. K. Matsuo, M. Kopecek, M.A. Nicoletti, J.P. Hatch, Y. Watanabe, F.G. Nery, G. Zunta-Soares, and J.C. Soares New structural brain imaging endophenotype in bipolar disorder Mol. Psychiatry 17 2012 412 420
56. M.J. McCarthy, S. Liang, A.D. Spadoni, J.R. Kelsoe, and A.N. Simmons Whole brain expression of bipolar disorder associated genes: structural and genetic analyses PLoS One 9 6 2014 10.1371/journal.pone.0100204
57. C. McDonald, E.T. Bullmore, P.C. Sham, X. Chitnis, H. Wickham, E. Bramon, and R.M. Murray Association of genetic risks for schizophrenia and bipolar disorder with specific and generic brain structural endophenotypes Arch. Gen. Psychiatry 61 2004 974 984
58. P. McGuffin, F. Rijsdijk, M. Andrew, P. Sham, R. Katz, and A. Cardno The heritability of bipolar affective disorder and the genetic relationship to unipolar depression Arch. Gen. Psychiatry 60 2003 497 502
59. A. Mechelli, C.J. Price, K.J. Friston, and J. Ashburner Voxel-based morphometry of the human brain: methods and applications Curr. Med. Imaging Rev. 1 2005 105 113
60. K.R. Merikangas, R. Jin, J.-P. He, R.C. Kessler, S. Lee, N.A. Sampson, M.C. Viana, L.H. Andrade, C. Hu, E.G. Karam, M. Ladea, M.E. Medina-Mora, Y. Ono, J. Posada-Villa, R. Sagar, J.E. Wells, and Z. Zarkov Prevalence and correlates of bipolar spectrum disorder in the world mental health survey initiative Arch. Gen. Psychiatry 68 2011 241 251
61. N.P. Mills, M.P. DelBello, C.M. Adler, and S.M. Strakowski MRI analysis of cerebellar vermal abnormalities in bipolar disorder Am. J. Psychiatry 162 2005 1530 1532
62. M.T. Mitterschiffthaler, C.H.Y. Fu, J.A. Dalton, C.M. Andrew, and S.C.R. Williams A functional MRI study of happy and sad affective states induced by classical music Hum. Brain Mapp. 28 2007 1150 1162
63. G.J. Moore, B.M. Cortese, D.A. Glitz, C. Zajac-Benitez, J.A. Quiroz, T.W. Uhde, W.C. Drevets, and H.K. Manji A longitudinal study of the effects of lithium treatment on prefrontal and subgenual prefrontal gray matter volume in treatment-responsive bipolar disorder patients J. Clin. Psychiatry 70 2009 699 705
64. T.W.J. Moorhead, J. McKirdy, J.E.D. Sussmann, J. Hall, S.M. Lawrie, E.C. Johnstone, and A.M. McIntosh Progressive gray matter loss in patients with bipolar disorder Biol. Psychiatry 62 2007 894 900
65. C.J. Murray, and A.D. Lopez Mortality by cause for eight regions of the world: global burden of disease study Lancet 349 1997 1269 1276
66. H.A. Nasrallah, C.G. Jacoby, and M. McCalley-Whitters Cerebellar atrophy in schizophrenia and mania Lancet 1 1981 1102
67. H.A. Nasrallah, M. McCalley Whitters, and C.G. Jacoby Cortical atrophy in schizophrenia and mania: a comparative CT study J. Clin. Psychiatry 43 1982 439 441
68. F.G. Nery, E.S. Monkul, and B. Lafer Gray matter abnormalities as brain structural vulnerability factors for bipolar disorder: a review of neuroimaging studies of individuals at high genetic risk for bipolar disorder Aust. N.Z. J. Psychiatry 47 2013 1124 1135
69. T.E. Nichols Multiple testing corrections, nonparametric methods, and random field theory Neuroimage 62 2 2012 811 815
70. V. Oertel-Knöchel, B. Reinke, R. Feddern, A. Knake, C. Knöchel, D. Prvulovic, J. Pantel, and D.E. Linden Episodic memory impairments in bipolar disorder are associated with functional and structural brain changes Bipolar Disord. 16 2014 830 845
71. N. Ramnani The primate cortico-cerebellar system: anatomy and function Nat. Rev. Neurosci. 7 2006 511 522
72. M. Rapoport The role of the cerebellum in cognition and behavior: a selective review J. Neuropsychiatry Clin. Neurosci. 12 2000 193 198
73. G. Roberts, M.J. Green, M. Breakspear, C. McCormack, A. Frankland, A. Wright, F. Levy, R. Lenroot, H.N. Chan, and P.B. Mitchell Reduced inferior frontal gyrus activation during response inhibition to emotional stimuli in youth at high risk of bipolar disorder Biol. Psychiatry 74 2013 55 61
74. J.D. Schmahmann From movement to thought: anatomic substrates of the cerebellar contribution to cognitive processing Hum. Brain Mapp. 4 1996 174 198
75. J.D. Schmahmann, and J.C. Sherman The cerebellar cognitive affective syndrome Brain 121 1998 561 579
76. J.D. Schmahmann, and D. Caplan Cognition, emotion and the cerebellum Brain 129 2006 290 292
77. A.P.R. Smith, R.N.A. Henson, R.J. Dolan, and M.D. Rugg fMRI correlates of the episodic retrieval of emotional contexts Neuroimage 22 2004 868 878
78. J.W. Smoller, and C.T. Finn Family, twin, and adoption studies of bipolar disorder Am. J. Med. Genet. C: Semin. Med. Genet. 123C 2003 48 58
79. A.C. Stanfield, T.W.J. Moorhead, D.E. Job, J. McKirdy, J.E.D. Sussmann, J. Hall, S. Giles, E.C. Johnstone, S.M. Lawrie, and A.M. McIntosh Structural abnormalities of ventrolateral and orbitofrontal cortex in patients with familial bipolar disorder Bipolar Disord. 11 2009 135 144
80. D. Swick, V. Ashley, and A.U. Turken Left inferior frontal gyrus is critical for response inhibition BMC Neurosci. 9 2008 102
81. W.L. Tseng, B.L. Bones, R.R. Kayser, A.K. Olsavsky, S.J. Fromm, D.S. Pine, E. Leibenluft, and M.A. Brotman An fMRI study of emotional face encoding in youth at risk for bipolar disorder Eur. Psychiatry 30 2015 94 98
82. A.C. Van der Schot, R. Vonk, R.M. Brouwer, G.C.M. van Baal, R.G.H. Brans, N.E.M. van Haren, H.G. Schnack, D.I. Boomsma, W.A. Nolen, H.E. Hulshoff Pol, and R.S. Kahn Genetic and environmental influences on focal brain density in bipolar disorder Brain 133 2010 3080 3092
83. D.R. Watson, J.M.E. Anderson, F. Bai, S.L. Barrett, T.M. McGinnity, C.C. Mulholland, T.M. Rushe, and S.J. Cooper A voxel based morphometry study investigating brain structural changes in first episode psychosis Behav. Brain Res. 227 2012 91 99
84. K. Yucel, M.C. McKinnon, V.H. Taylor, K. Macdonald, M. Alda, L.T. Young, and G.M. MacQueen Bilateral hippocampal volume increases after long-term lithium treatment in patients with bipolar disorder: a longitudinal MRI study Psychopharmacology 195 2007 357 367
85. M.E. Zimmerman, M.P. DelBello, G.E. Getz, P.K. Shear, and S.M. Strakowski Anterior cingulate subregion volumes and executive function in bipolar disorder Bipolar Disord. 8 2006 281 288
86. S. Zola-Morgan, L.R. Squire, D.G. Amaral, and W.A. Suzuki Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment J. Neurosci. 9 1989 4355 4370