Psychiatry Research: Neuroimaging
Volume 162, Issue 1 , Pages 27-37 , 15 January 2008

Evidence for deficient modulation of amygdala response by prefrontal cortex in bipolar mania

  • Lara C. Foland

      Affiliations

    • Laboratory of NeuroImaging, Department of Neurology, University of California, Los Angeles, CA, USA
  • ,
  • Lori L. Altshuler

      Affiliations

    • Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, CA, USA
    • Department of Psychiatry, VA Greater Los Angeles Healthcare System, West Los Angeles Healthcare Center, Los Angeles, CA, USA
    • Corresponding Author InformationCorresponding author. UCLA Neuropsychiatric Institute and Hospital, 300 Medical Plaza, Suite 1544, Box 957057, Los Angeles, CA 90095-7507, USA. Tel.: +1 310 794 9911; fax: +1 310 794 9915.
  • ,
  • Susan Y. Bookheimer

      Affiliations

    • Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, CA, USA
    • Ahmanson-Lovelace Brain Mapping Center, UCLA School of Medicine, Los Angeles, CA, USA
  • ,
  • Naomi Eisenberger

      Affiliations

    • Cousins Center for Psychoneuroimmunology, University of California, Los Angeles, CA, USA
  • ,
  • Jennifer Townsend

      Affiliations

    • Ahmanson-Lovelace Brain Mapping Center, UCLA School of Medicine, Los Angeles, CA, USA
  • ,
  • Paul M. Thompson

      Affiliations

    • Laboratory of NeuroImaging, Department of Neurology, University of California, Los Angeles, CA, USA

Received 2 November 2006 ,Revised 10 March 2007 ,Accepted 8 April 2007.

References 

  1. al Maskati HA, Zbrozyna AW. Stimulation in prefrontal cortex area inhibits cardiovascular and motor components of the defense reaction in rats. Journal of the Autonomic Nervous System. 1989;28:117–125
  2. Altshuler LL, Bartzokis G, Grieder T, Curran J, Mintz J. Amygdala enlargement in bipolar disorder and hippocampal reduction in schizophrenia: an MRI study demonstrating neuroanatomic specificity. Archives of General Psychiatry. 1998;55:663–664
  3. Altshuler LL, Bookheimer SY, Proenza MA, Townsend J, Sabb F, Firestine A, et al. Increased amygdala activation during mania: a functional magnetic resonance imaging study. American Journal of Psychiatry. 2005;162:1211–1213
  4. Altshuler LL, Bookheimer SY, Townsend J, Proenza MA, Eisenberger N, Sabb F, et al. Blunted activation in orbitofrontal cortex during mania: a functional magnetic resonance imaging study. Biological Psychiatry. 2005;58:763–769
  5. Amaral D, Price J, Pitakanen A, Carmichael S. Anatomical organization of the primate amygdaloid complex. In:  Aggleton J editors. The Amygdala. New York: Wiley-Liss; 1992;
  6. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th edition (DSM-IV). Washington DC: American Psychiatric Association; 1994;
  7. Blumberg HP, Stern E, Ricketts S, Martinez D, de Asis J, White T, et al. Rostral and orbital prefrontal cortex dysfunction in the manic state of bipolar disorder. American Journal of Psychiatry. 1999;156:1986–1988
  8. Blumberg HP, Leung HC, Skudlarski P, Lacadie CM, Fredericks CA, Harris BC, et al. A functional magnetic resonance imaging study of bipolar disorder: state- and trait-related dysfunction in ventral prefrontal cortices. Archives of General Psychiatry. 2003;60:601–609
  9. Blumberg HP, Donegan NH, Sanislow CA, Collins S, Lacadie C, Skudlarski P, et al. Preliminary evidence for medication effects on functional abnormalities in the amygdala and anterior cingulate in bipolar disorder. Psychopharmacology. 2005;183:308–313
  10. Brambilla P, Harenski K, Nicoletti M, Sassi RB, Mallinger AG, Frank E, et al. MRI investigation of temporal lobe structures in bipolar patients. Journal of Psychiatric Research. 2003;37:287–295
  11. Cavada C, Company T, Tejedor J, Cruz-Rizzolo RJ, Reinoso-Suarez F. The anatomical connections of the macaque monkey orbitofrontal cortex: a review. Cerebral Cortex. 2000;10:220–242
  12. Chen CH, Lennox B, Jacob R, Calder A, Lupson V, Bisbrown-Chippendale R, et al. Explicit and implicit facial affect recognition in manic and depressed states of bipolar disorder: a functional magnetic resonance imaging study. Biological Psychiatry. 2006;59:31–39
  13. Cooney RE, Atlas LY, Joormann J, Eugene F, Gotlib IH. Amygdala activation in the processing of neutral faces in social anxiety disorder: is neutral really neutral?. Psychiatry Research. 2006;148:55–59
  14. Critchley H, Daly E, Phillips M, Brammer M, Bullmore E, Williams S, et al. Explicit and implicit neural mechanisms for processing of social information from facial expressions: a functional magnetic resonance imaging study. Human Brain Mapping. 2000;9:93–105
  15. Dannlowski U, Ohrmann P, Bauer J, Kugel H, Arolt V, Heindel W, et al. Amygdala reactivity predicts automatic negative evaluations for facial emotions. Psychiatry Research. 2007;154:13–20
  16. Das P, Flynn G, Harris AWF, Kemp AH, Liddell BJ, Whitford T, et al. Dysfunctions in the direct and indirect thalamo-amygdala pathways during facial emotion perception in schizophrenia: a functional connectivity approach. Organization for Human Brain Mapping Abstracts. 2006;Florence, Italy
  17. Dias R, Robbins TW, Roberts AC. Dissociation in prefrontal cortex of affective and attentional shifts. Letters to Nature. 1996;380:69–72
  18. Egner T, Hirsch J. The neural correlates and functional integration of cognitive control in a Stroop task. Neuroimage. 2004;24:539–547
  19. Ekman P, Friesen WV. Pictures of Facial Affect. Palo Alto: Consulting Psychologists Press; 1976;
  20. Elliott R, Ogilvie A, Rubinsztein JS, Calderon G, Dolan RJ, Sahakian BJ. Abnormal ventral frontal response during performance of an affective go/no go task in patients with mania. Biological Psychiatry. 2004;55:1163–1170
  21. Franguo S. The Maudsley bipolar disorder project. Epilepsia. 2005;46:19–25
  22. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage. 1997;6:218–229
  23. Gaillard WD, Zeffiro T, Fazilat S, DeCarli C, Theodore WH. Effect of valproate on cerebral metabolism and blood flow: an 18F-2-deoxyglucose and 15O water positron emission tomography study. Epilepsia. 1996;37:515–521
  24. Getz GE, Shear PK, Strakowski SM. Facial affect recognition deficits in bipolar disorder. Journal of the International Neuropsychological Society. 2003;9:623–632
  25. Ghashghaei H, Barbas H. Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience. 2002;115:1261–1279
  26. Gitelman DR, Penny WD, Ashburner J, Friston KJ. Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage. 2003;19:200–207
  27. Hamilton M. A rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry. 1960;23:56–62
  28. Hariri AR, Bookheimer SY, Mazziotta JC. Modulating emotional responses: effects of a neocortical network on the limbic system. Neuroreport. 2000;11:43–48
  29. Hariri AR, Mattay VS, Tessitore A, Fera F, Weinberger DR. Neocortical modulation of the amygdala response to fearful stimuli. Biological Psychiatry. 2003;53:494–501
  30. Horwitz B. The elusive concept of brain connectivity. Neuroimage. 2003;19:466–470
  31. Horwitz B, Tagamets MA, McIntosh AR. Neural modeling, functional brain imaging, and cognition. Trends in Cognitive Sciences. 1999;3:91–98
  32. Lawrence NS, Williams AM, Surguladze S, Giampietro V, Brammer MJ, Andrew C, et al. Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biological Psychiatry. 2004;55:578–587
  33. Leiderman DB, Balish M, Bromfield EB, Theodore WH. Effect of valproate on human cerebral glucose metabolism. Epilepsia. 1991;32:417–422
  34. Lembke A, Ketter TA. Impaired recognition of facial emotion in mania. American Journal of Psychiatry. 2002;159:302–304
  35. Lennox BR, Jacob R, Calder AJ, Lupson V, Bullmore ET. Behavioural and neurocognitive responses to sad facial affect are attenuated in patients with mania. Psychological Medicine. 2004;34:795–802
  36. Lieberman MD, Hariri A, Jarcho JM, Eisenberger NI, Bookheimer SY. An fMRI investigation of race-related amygdala activity in African–American and Caucasian–American individuals. Nature Neuroscience. 2005;6:720–722
  37. Lieberman, M.D., Eisenberger, N.I., Crockett, M.J., Tom, S.M., Pfeifer, J.H., Way, B.M., 2007. Putting feelings into words: affect labeling disrupts amygdala activity to affective stimuli. Psychological Science 18, 421–428.
  38. Lopez-Larson MP, DelBello MP, Zimmerman ME, Schwiers ML, Strakowski SM. Regional prefrontal gray and white matter abnormalities in bipolar disorder. Biological Psychiatry. 2002;52:93–100
  39. Lovejoy MC, Steuerwald BL. Subsyndromal unipolar and bipolar disorders: comparisons on positive and negative affect. Journal of Abnormal Psychology. 1995;104:381–384
  40. Lyoo IK, Kim MJ, Stoll AL, Demopulos CM, Parow AM, Dager SR, et al. Frontal lobe gray matter density decreases in bipolar I disorder. Biological Psychiatry. 2004;55:648–651
  41. Malhi G, Lagopoulos J, Sachdev P, Ivanovskia B, Shniere R. An emotional stroop functional MRI study of euthymic bipolar disorder. Bipolar Disorders. 2005;7:58–69
  42. Meyer-Lindenberg A, Poline JB, Kohn PD, Holt JL, Egan MF, Weinberger DR, et al. Evidence for abnormal cortical functional connectivity during working memory in schizophrenia. American Journal of Psychiatry. 2001;158:1809–1817
  43. New, A.S., Hazlett, E.A., Buchsbaum, M.S., Goodman, M., Mitelman, S.A., Newmark, R., Trisdorfer, R., Haznedar, M.M., Koenigsberg, H.W., Flory, J., Siever, L.J., 2007. Amygdala prefrontal disconnection in borderline personality disorder. Neuropsychopharmacology 32, 1629–1640.
  44. Ochsner KN, Bunge SA, Gross JJ, Gabrieli JD. Rethinking feelings: an fMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience. 2002;15:1215–1529
  45. Ochsner KN, Ray RD, Cooper JC, Robertson ER, Chopra S, Gabrieli JD, et al. For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. Neuroimage. 2004;23:483–499
  46. Oliver DW, Dormehl IC. Cerebral blood flow effects of sodium valproate in drug combinations in the baboon model. Arzneimittelforschung. 1998;48:1058–1063
  47. Orban P, Rauchs G, Balteau E, Degueldre C, Luxen A, Maquet P, et al. Sleep after spatial learning promotes covert reorganization of brain activity. Proceedings of the National Academy of Sciences of the United States of America. 2006;103:7124–7129
  48. Pessoa L, McKenna M, Gutierrez E, Ungerleider LG. Neural processing of emotional faces requires attention. Proceedings of the National Academy of Sciences of the United States of America. 2002;99:11458–11463
  49. Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski BA, Munoz KE, Kolachana BS, et al. 5-HTTLPR polymorphism impacts human cingulate–amygdala interactions: a genetic susceptibility mechanism for depression. Nature Neuroscience. 2005;8:828–834
  50. Phan KL, Fitzgerald DA, Nathan PJ, Moore GJ, Uhde TW, Tancer ME. Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study. Biological Psychiatry. 2005;57:210–219
  51. Rich BA, Vinton DT, Roberson-Nay R, Hommer RE, Berghorst LH, McClure EB, et al. Limbic hyperactivation during processing of neutral facial expressions in children with bipolar disorder. Proceedings of the National Academy of Sciences of the United States of America. 2006;103:8900–8905
  52. Rubinsztein JS, Fletcher PC, Rogers RD, Ho LW, Aigbirhio FI, Paykel ES, et al. Decision-making in mania: a PET study. Brain. 2001;124:2550–6253
  53. Starkstein SE, Robinson RG. Mechanisms of disinhibition after brain lesions. Journal of Nervous and Mental Disease. 1997;182:108–114
  54. Stephan KE, Marshall JC, Friston KJ, Rowe JB, Ritzl A, Zilles K, et al. In: Lateralized cognitive processes and lateralized task control in the human brain. vol. 301:2003;p. 384–386
  55. Strakowski SM, DelBello MP, Sax KW, Zimmerman ME, Shear PK, Hawkins JM, et al. Brain magnetic resonance imaging of structural abnormalities in bipolar disorder. Archives of General Psychiatry. 1999;56:254–260
  56. Strakowski S, Adler C, Holland S, Mills N, DelBello M, Eliassen J. Abnormal fMRI brain activation in euthymic bipolar disorder patients during a counting Stroop interference task. American Journal of Psychiatry. 2005;162:1697–1705
  57. Theodore WH. PET: cerebral blood flow and glucose metabolism—pathophysiology and drug effects. Advances in Neurology. 2000;83:121–130
  58. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. Journal of Neuroscience. 2002;22:6810–6818
  59. Williams LM, Das P, Liddell BJ, Kemp AH, Rennie CJ, Gordon E. Mode of functional connectivity in amygdala pathways dissociates level of awareness for signals of fear. Journal of Neuroscience. 2006;26:9264–9271
  60. Woods RP, Grafton ST, Holmes CJ, Cherry SR, Mazziotta JC. Automated image registration: I. General methods and intrasubject, intramodality validation. Journal of Computer Assisted Tomography. 1998;22:139–152
  61. Young RC, Biggs JT, Ziegler VE, Meyer DA. A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry. 1978;133:429–435
  62. Yurgelun-Todd DA, Gruber SA, Kanayama G, Killgore WDS, Baird AA, Young AD. fMRI during affect discrimination in bipolar affective disorder. Bipolar Disorders. 2000;2:237–248

PII: S0925-4927(07)00087-X

doi: 10.1016/j.pscychresns.2007.04.007

Psychiatry Research: Neuroimaging
Volume 162, Issue 1 , Pages 27-37 , 15 January 2008