Disturbed cortico–amygdalar functional connectivity as pathophysiological correlate of working memory deficits in bipolar affective disorder

European Archives of Psychiatry and Clinical Neuroscience

Volumn 265, Issue 4, 2015, Pages 303-311

  Stegmayer, Katharina ^a   Usher, Juliana ^b   Trost, Sarah ^b   Henseler, Ilona ^c   Tost, Heike ^d   Rietschel, Marcella ^d   Falkai, Peter ^e   Gruber, Oliver ^b  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^c MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

^d CENTRAL INSTITUTE OF MENTAL HEALTH   (Germany)

^e LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

Amygdala; Euthymia; Functional coupling; Functional magnetic resonance imaging; Limbic system

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BILATERAL INTRAPARIETAL CORTEX; BIPOLAR DISORDER; BRAIN CORTEX; CEREBELLUM; CEREBELLUM VERMIS; CLINICAL ARTICLE; CONTROLLED STUDY; EXPERIMENTAL COGNITIVE TEST; FEMALE; FRONTAL EYE FIELD; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFERIOR FRONTAL GYRUS; INFERIOR PARIETAL LOBULE; INTRAPARIETAL SULCUS; LEFT TEMPOROPOLAR CORTEX; MALE; NEUROIMAGING; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RIGHT HEMISPHERE; STERNBERG ITEM RECOGNITION TASK; SUPPLEMENTARY MOTOR AREA; VENTRAL PALLIDUM; WORKING MEMORY; ANALYSIS OF VARIANCE; BLOOD; COMPLICATION; IMAGE PROCESSING; LEARNING; MEMORY DISORDERS; MIDDLE AGED; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PHOTOSTIMULATION; PHYSIOLOGY; PSYCHOLOGICAL RATING SCALE; PSYCHOPHYSICS; SHORT TERM MEMORY; VASCULARIZATION; YOUNG ADULT;

OXYGEN;

ADULT; AMYGDALA; ANALYSIS OF VARIANCE; BIPOLAR DISORDER; CEREBRAL CORTEX; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY DISORDERS; MEMORY, SHORT-TERM; MIDDLE AGED; NEURAL PATHWAYS; OXYGEN; PHOTIC STIMULATION; PSYCHIATRIC STATUS RATING SCALES; PSYCHOPHYSICS; VERBAL LEARNING; YOUNG ADULT;

EID: 84939417942     PISSN: 09401334     EISSN: 14338491     Source Type: Journal    
DOI: 10.1007/s00406-014-0517-5     Document Type: Article

References (55)

1. Phillips ML, Vieta E (2007) Identifying functional neuroimaging biomarkers of bipolar disorder: toward DSM-V. Schizophr Bull 33:893–904. doi:10.1093/schbul/sbm060
2. Wang F, Kalmar JH, He Y et al (2009) Functional and structural connectivity between the perigenual anterior cingulate and amygdala in bipolar disorder. Biol Psychiatry 66:516–521. doi:10.1016/j.biopsych.2009.03.023
3. Usher J, Leucht S, Falkai P, Scherk H (2010) Correlation between amygdala volume and age in bipolar disorder—a systematic review and meta-analysis of structural MRI studies. Psychiatry Res 182:1–8. doi:10.1016/j.pscychresns.2009.09.004
4. Yurgelun-Todd DA, Gruber SA, Kanayama G et al (2000) fMRI during affect discrimination in bipolar affective disorder. Bipolar Disord 2:237–248
5. Lawrence NS, Williams AM, Surguladze S et al (2004) Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biol Psychiatry 55:578–587. doi:10.1016/j.biopsych.2003.11.017
6. Malhi GS, Lagopoulos J, Ward PB et al (2004) Cognitive generation of affect in bipolar depression: an fMRI study. Eur J Neurosci 19:741–754
7. Rich BA, Vinton DT, Roberson-Nay R et al (2006) Limbic hyperactivation during processing of neutral facial expressions in children with bipolar disorder. Proc Natl Acad Sci USA 103:8900–8905. doi:10.1073/pnas.0603246103
8. Pavuluri MN, O’Connor MM, Harral E, Sweeney JA (2007) Affective neural circuitry during facial emotion processing in pediatric bipolar disorder. Biol Psychiatry 62:158–167. doi:10.1016/j.biopsych.2006.07.011
9. Bermpohl F et al (2009) A preliminary study of increased amygdala activation to positive affective stimuli in mania. Bipolar Disord 11(1):70–75. doi:10.1111/j.1399-5618.2008.00648.x
10. Blumberg HP, Martin A, Kaufman J et al (2003) Frontostriatal abnormalities in adolescents with bipolar disorder: preliminary observations from functional MRI. Am J Psychiatry 160:1345–1347
11. Blumberg HP, Leung H-C, Skudlarski P et al (2003) A functional magnetic resonance imaging study of bipolar disorder: state- and trait-related dysfunction in ventral prefrontal cortices. Arch Gen Psychiatry 60:601–609. doi:10.1001/archpsyc.60.6.601
12. Gruber SA, Rogowska J, Yurgelun-Todd DA (2004) Decreased activation of the anterior cingulate in bipolar patients: an fMRI study. J Affect Disord 82:191–201. doi:10.1016/j.jad.2003.10.010
13. MacQueen GM, Hajek T, Alda M (2005) The phenotypes of bipolar disorder: relevance for genetic investigations. Mol Psychiatry 10:811–826. doi:10.1038/sj.mp.4001701
14. Kronhaus DM, Lawrence NS, Williams AM et al (2006) Stroop performance in bipolar disorder: further evidence for abnormalities in the ventral prefrontal cortex. Bipolar Disord 8:28–39. doi:10.1111/j.1399-5618.2006.00282.x
15. Melcher T, Wolter S, Falck S et al (2013) Common and disease-specific dysfunctions of brain systems underlying attentional and executive control in schizophrenia and bipolar disorder. Eur Arch Psychiatry Clin Neurosci. doi:10.1007/s00406-013-0445-9
16. Gruber O, von Cramon DY (2001) Domain-specific distribution of working memory processes along human prefrontal and parietal cortices: a functional magnetic resonance imaging study. Neurosci Lett 297:29–32
17. Gruber O, von Cramon DY (2003) The functional neuroanatomy of human working memory revisited. Evidence from 3-T fMRI studies using classical domain-specific interference tasks. NeuroImage 19:797–809
18. Amaral DG, Price JL (1984) Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 230:465–496. doi:10.1002/cne.902300402
19. Barbas H, De Olmos J (1990) Projections from the amygdala to basoventral and mediodorsal prefrontal regions in the rhesus monkey. J Comp Neurol 300:549–571. doi:10.1002/cne.903000409
20. Stefanacci L, Suzuki WA, Amaral DG (1996) Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys. J Comp Neurol 375:552–582. doi:10.1002/(SICI)1096-9861(19961125)375:4<552:AID-CNE2>3.0.CO;2-0
21. Ghashghaei HT, Barbas H (2002) Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115:1261–1279
22. Stein JL, Wiedholz LM, Bassett DS et al (2007) A validated network of effective amygdala connectivity. NeuroImage 36:736–745. doi:10.1016/j.neuroimage.2007.03.022
23. Rolls ET (2005) Emotion explained. University Press, Oxford
24. Dannlowski U et al (2007) Amygdala reactivity predicts automatic negative evaluations for facial emotions. Psychiatry Res 154(1):13–20
25. Kim MJ, Loucks RA, Palmer AL et al (2011) The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav Brain Res 223:403–410. doi:10.1016/j.bbr.2011.04.025
26. Ochsner KN, Ray RD, Cooper JC et al (2004) For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage 23:483–499. doi:10.1016/j.neuroimage.2004.06.030
27. Weinberger NA, Metherate R, McKenna T et al (1990) Neural adaptive information processing: a preliminary model of receptive-field plasticity in auditory cortex during Pavlovian conditioning. In: Gabriel M, Moore J (eds) Learning and computational neuroscience: foundations of adaptive networks. The MIT Press, Cambridge, pp 91–138
28. Pare D, Quirk GJ, Ledoux JE (2004) New vistas on amygdala networks in conditioned fear. J Neurophysiol 92:1–9
29. Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175–187
30. Gruber O, Tost H, Henseler I et al (2010) Pathological amygdala activation during working memory performance: evidence for a pathophysiological trait marker in bipolar affective disorder. Hum Brain Mapp 31:115–125. doi:10.1002/hbm.20849
31. Trost S, Gruber O (2012) Evidence for a double dissociation of articulatory rehearsal and non-articulatory maintenance of phonological information in human verbal working memory. Neuropsychobiology 65:133–140. doi:10.1159/000332335
32. Gruber O (2001) Effects of domain-specific interference on brain activation associated with verbal working memory task performance. Cereb Cortex 11(11):1047–1055. doi:10.1093/cercor/11.11.1047
33. Friston KJ, Buechel C, Fink GR et al (1997) Psychophysiological and modulatory interactions in neuroimaging. NeuroImage 6:218–229. doi:10.1006/nimg.1997.0291
34. Penny WD, Holmes AJ (2003) Random-effects analysis. Academic Press, San Diego
35. Pessoa L (2008) On the relationship between emotion and cognition. Nat Rev Neurosci 9:148–158. doi:10.1038/nrn2317
36. McIntyre CK, Marriott LK, Gold PE (2003) Cooperation between memory systems: acetylcholine release in the amygdala correlates positively with good performance on a hippocampus-dependent task. Behav Neurosci 117:320–326
37. Curcić-Blake B, Swart M, Aleman A (2012) Bidirectional information flow in frontoamygdalar circuits in humans: a dynamic causal modeling study of emotional associative learning. Cereb Cortex 22(2):436–445. doi:10.1093/cercor/bhr124
38. Banks SJ, Eddy KT, Angstadt M et al (2007) Amygdala-frontal connectivity during emotion regulation. Soc Cogn Affect Neurosci 2:303–312. doi:10.1093/scan/nsm029
39. Moses-Kolko EL, Perlman SB, Wisner KL et al (2010) Abnormally reduced dorsomedial prefrontal cortical activity and effective connectivity with amygdala in response to negative emotional faces in postpartum depression. Am J Psychiatry 167:1373–1380. doi:10.1176/appi.ajp.2010.09081235
40. Versace A, Thompson WK, Zhou D et al (2010) Abnormal left and right amygdala–orbitofrontal cortical functional connectivity to emotional faces: state versus trait vulnerability markers of depression in bipolar disorder. Biol Psychiatry 67:422–431. doi:10.1016/j.biopsych.2009.11.025
41. Anand A, Li Y, Wang Y et al (2009) Resting state corticolimbic connectivity abnormalities in unmedicated bipolar disorder and unipolar depression. Psychiatry Res 171:189–198. doi:10.1016/j.pscychresns.2008.03.012
42. Rosenkranz JA, Moore H, Grace AA (2003) The prefrontal cortex regulates lateral amygdala neuronal plasticity and responses to previously conditioned stimuli. J Neurosci Off J Soc Neurosci 23:11054–11064
43. Chepenik LG, Raffo M, Hampson M et al (2010) Functional connectivity between ventral prefrontal cortex and amygdala at low frequency in the resting state in bipolar disorder. Psychiatry Res 182:207–210. doi:10.1016/j.pscychresns.2010.04.002
44. Foland LC, Altshuler LL, Bookheimer SY et al (2008) Evidence for deficient modulation of amygdala response by prefrontal cortex in bipolar mania. Psychiatry Res 162:27–37. doi:10.1016/j.pscychresns.2007.04.007
45. Gray JR (2001) Emotional modulation of cognitive control: approach-withdrawal states double-dissociate spatial from verbal two-back task performance. J Exp Psychol Gen 130:436–452
46. Northoff G, Heinzel A, Bermpohl F et al (2004) Reciprocal modulation and attenuation in the prefrontal cortex: an fMRI study on emotional–cognitive interaction. Hum Brain Mapp 21:202–212. doi:10.1002/hbm.20002
47. Dolcos F, McCarthy G (2006) Brain systems mediating cognitive interference by emotional distraction. J Neurosci Off J Soc Neurosci 26:2072–2079. doi:10.1523/JNEUROSCI.5042-05.2006
48. Melcher T, Born C, Gruber O (2011) How negative affect influences neural control processes underlying the resolution of cognitive interference: an event-related fMRI study. Neurosci Res 70:415–427. doi:10.1016/j.neures.2011.05.007
49. Foland LC, Altshuler LL, Sugar CA, Lee AD et al (2008) Increased volume of the amygdala and hippocampus in bipolar patients treated with lithium. NeuroReport 19:221–224
50. Haldane M, Jogia J, Cobb A, Kozuch E, Kumari V, Frangou S (2008) Changes in brain activation during working memory and facial recognition tasks in patients with bipolar disorder with Lamotrigine monotherapy. Eur Neuropsychopharmacol 18:48–54
51. Hafeman DM, Chang KD, Garrett AS, Sanders EM, Phillips ML (2012) Effects of medication on neuroimaging findings in bipolar disorder: an updated review. Bipolar Disord 14:375–410
52. Lindquist MA, Wager TD (2008) Spatial smoothing in fMRI using prolate spheroidal wave functions. Hum Brain Mapp 29:1276–1287
53. Sacchet MD, Knutson B (2012) Spatial smoothing systematically biases the localization of reward-related brain activity. Neuroimage 66C:270–277
54. Dagli MS, Ingeholm JE, Haxby JV (1999) Localization of cardiac-induced signal change in fMRI. Neuroimage 9:407–415
55. Windischberger C, Langenberger H, Sycha T, Tschernko EM, Fuchsjager-Mayerl G, Schmetterer L, Moser E (2002) On the origin of respiratory artifacts in BOLD-EPI of the human brain. Magn Reson Imaging 20:575–582