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Distinct neural mechanisms of emotional processing in prolonged grief disorder

Published online by Cambridge University Press:  07 January 2020

Richard A. Bryant Open the ORCID record for Richard A. Bryant [Opens in a new window] ,
Elpiniki Andrew  and
Mayuresh S. Korgaonkar
Richard A. Bryant*
Affiliation:
School of Psychology, University of New South Wales, Sydney, Australia Brain Dynamics Centre, Westmead Institute of Medical Research, Westmead, Australia
Elpiniki Andrew
Affiliation:
School of Psychology, University of New South Wales, Sydney, Australia Brain Dynamics Centre, Westmead Institute of Medical Research, Westmead, Australia
Mayuresh S. Korgaonkar
Affiliation:
Brain Dynamics Centre, Westmead Institute of Medical Research, Westmead, Australia Sydney Medical School, University of Sydney, Sydney, Australia
*
Author for correspondence: Richard A. Bryant, E-mail: r.bryant@unsw.edu.au
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Abstract

Background

Prolonged grief disorder (PGD) has recently been recognized as a separate psychiatric diagnosis, despite controversy over the extent to which it is distinctive from posttraumatic stress disorder (PTSD) and major depressive disorder (MDD).

Methods

This study investigated distinctive neural processes underpinning emotion processing in participants with PGD, PTSD, and MDD with functional magnetic resonance study of 117 participants that included PGD (n = 21), PTSD (n = 45), MDD (n = 26), and bereaved controls (BC) (n = 25). Neural responses were measured across the brain while sad, happy, or neutral faces were presented at both supraliminal and subliminal levels.

Results

PGD had greater activation in the pregenual anterior cingulate cortex (pgACC), bilateral insula, bilateral dorsolateral prefrontal cortices and right caudate and also greater pgACC–right pallidum connectivity relative to BC during subliminal processing of happy faces. PGD was distinct relative to both PTSD and MDD groups with greater recruitment of the medial orbitofrontal cortex during supraliminal processing of sad faces. PGD were also distinct relative to MDD (but not PTSD) with greater activation in the left amygdala, caudate, and putamen during subliminal presentation of sad faces. There was no distinction between PGD, PTSD, and MDD during processing of happy faces.

Conclusions

These results provide initial evidence of distinct neural profiles of PGD relative to related psychopathological conditions, and highlight activation of neural regions implicated in reward networks. This pattern of findings validates current models of PGD that emphasize the roles of yearning and appetitive processes in PGD.

Keywords

Diagnosisfunctional magnetic resonance imagingposttraumatic stress disorderprolonged grief disorder
Type
Original Article
Information
Psychological Medicine , Volume 51 , Issue 4 , March 2021 , pp. 587 - 595
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Copyright
Copyright © Cambridge University Press 2020

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References

Almeida, J. R., Versace, A., Hassel, S., Kupfer, D. J., & Phillips, M. L. (2010). Elevated amygdala activity to sad facial expressions: A state marker of bipolar but not unipolar depression. Biological Psychiatry, 67, 414–421.CrossRefGoogle Scholar
Andersson, J. L., Jenkinson, M., & Smith, S. M. (2007a) Non-linear optimisation. FMRIB technical report TR07JA1. Retrieved March 10, 2017, from www.fmrib.ox.ac.uk/analysis/techrep.Google Scholar
Andersson, J. L., Jenkinson, M., & Smith, S. M. (2007b) Non-linear registration and spatial normalisation. FMRIB technical report TR07JA2. Retrieved March 10, 2017, from www.frmrib.ox.ac.uk/analysis/techrep.Google Scholar
Arizmendi, B., Kaszniak, A. W., & O'Connor, M. F. (2016). Disrupted prefrontal activity during emotion processing in complicated grief: An fMRI investigation. Neuroimage, 124, 968–976.CrossRefGoogle ScholarPubMed
Aron, A., Fisher, H., Mashek, D. J., Strong, G., Li, H., & Brown, L. L. (2005). Reward, motivation, and emotion systems associated with early-stage intense romantic love. Journal of Neurophysiology, 94, 327–337.CrossRefGoogle ScholarPubMed
Beck, A. T., Steer, R. A., & Brown, G. K. (1996). Beck Depression Inventory-Second Edition. San Antonio, TX: The Psychological Corporation.Google Scholar
Benjet, C., Bromet, E., Karam, E. G., Kessler, R. C., McLaughlin, K. A., Ruscio, A. M., … Koenen, K. C. (2016). The epidemiology of traumatic event exposure worldwide: Results from the World Mental Health Survey Consortium. Psychological Medicine 46, 327–343.CrossRefGoogle ScholarPubMed
Blake, D. D., Weathers, F., Nagy, L. M., Kaloupek, D. G., Gusman, F. D., Charney, D. S., et al. (1995). The development of a clinician administered PTSD scale. Journal of Traumatic Stress, 8, 75–90.CrossRefGoogle ScholarPubMed
Boelen, P. A., & van den Bout, J. (2005). Complicated grief, depression, and anxiety as distinct postloss syndromes: A confirmatory factor analysis study. American Journal of Psychiatry, 162, 2175–2177.CrossRefGoogle ScholarPubMed
Boelen, P. A., van den Hout, M. A., & van den Bout, J. (2006). A cognitive-behavioral conceptualization of complicated grief. Clinical Psychology: Science and Practice, 13, 109–128.Google Scholar
Dallimore, J. E., Mickiewicz, A. L., & Napier, T. C. (2006). Intra-ventral pallidal glutamate antagonists block expression of morphine-induced place preference. Behavioral Neuroscience, 120, 1103–1114.CrossRefGoogle ScholarPubMed
Drevets, W. C. (2001). Neuroimaging and neuropathological studies of depression: Implications for the cognitive-emotional features of mood disorders. Current Opinion in Neurobiology, 11, 240–249.CrossRefGoogle ScholarPubMed
Felmingham, K. L., Falconer, E. M., Williams, L., Kemp, A. H., Allen, A., Peduto, A., et al. (2014). Reduced amygdala and ventral striatal activity to happy faces in PTSD is associated with emotional numbing. PLoS ONE, 9, e103653.CrossRefGoogle ScholarPubMed
Filkowski, M. M., & Haas, B. W. (2017). Rethinking the use of neutral faces as a baseline in fMRI neuroimaging studies of axis-I psychiatric disorders. Journal of Neuroimaging, 27, 281–291.CrossRefGoogle ScholarPubMed
Fisher, H. E., Brown, L. L., Aron, A., Strong, G., & Mashek, D. (2010). Reward, addiction, and emotion regulation systems associated with rejection in love. Journal of Neurophysiology, 104, 51–60.CrossRefGoogle ScholarPubMed
Freed, P. J., Yanagihara, T. K., Hirsch, J., & Mann, J. J. (2009). Neural mechanisms of grief regulation. Biological Psychiatry, 66, 33–40.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Placentino, A., Carletti, F., Landi, P., Allen, P., Surguladze, S., et al. (2009). Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry and Neuroscience, 34, 418–432.Google ScholarPubMed
Golden, A.-M., & Dalgleish, T. (2010). Is prolonged grief distinct from bereavement-related posttraumatic stress? Psychiatry Research, 178, 336–341.CrossRefGoogle ScholarPubMed
Groves, S. J., Pitcher, T. L., Melzer, T. R., Jordan, J., Carter, J. D., Malhi, G. S., et al. (2018). Brain activation during processing of genuine facial emotion in depression: Preliminary findings. Journal of Affective Disorders, 225, 91–96.CrossRefGoogle ScholarPubMed
Gundel, H., O'Connor, M. F., Littrell, L., Fort, C., & Lane, R. D. (2003). Functional neuroanatomy of grief: An FMRI study. American Journal of Psychiatry, 160, 1946–1953.CrossRefGoogle Scholar
Haber, S. N., & Knutson, B. (2010). The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology, 35, 4–26.CrossRefGoogle ScholarPubMed
Keedwell, P. A., Andrew, C., Williams, S. C., Brammer, M. J., & Phillips, M. (2005). The neural correlates of anhedonia in major depressive disorder. Biological Psychiatry, 58, 843–853.CrossRefGoogle ScholarPubMed
Kersting, A., Brähler, E., Glaesmer, H., & Wagner, B. (2011). Prevalence of complicated grief in a representative population-based sample. Journal of Affective Disorders, 131, 339–343.CrossRefGoogle Scholar
Kersting, A., Ohrmann, P., Pedersen, A., Kroker, K., Samberg, D., Bauer, J., et al. (2009). Neural activation underlying acute grief in women after the loss of an unborn child. American Journal of Psychiatry, 166, 1402–1410.CrossRefGoogle ScholarPubMed
Kirby, L. A. J., & Robinson, J. L. (2017). Affective mapping: An activation likelihood estimation (ALE) meta-analysis. Brain & Cognition, 118, 137–148.CrossRefGoogle ScholarPubMed
Kober, H., Barrett, L. F., Joseph, J., Bliss-Moreau, E., Lindquist, K., & Wager, T. D. (2008). Functional grouping and cortical-subcortical interactions in emotion: A meta-analysis of neuroimaging studies. Neuroimage, 42, 998–1031.CrossRefGoogle ScholarPubMed
Koenen, K. C., Fu, Q. J., Ertel, K., Lyons, M. J., Eisen, S. A., True, W. R., et al. (2008). Common genetic liability to major depression and posttraumatic stress disorder in men. Journal of Affective Disorders, 105, 109–115.CrossRefGoogle ScholarPubMed
Korgaonkar, M. S., Grieve, S. M., Etkin, A., Koslow, S. H., & Williams, L. M. (2013). Using standardized fMRI protocols to identify patterns of prefrontal circuit dysregulation that are common and specific to cognitive and emotional tasks in major depressive disorder: First wave results from the iSPOT-D study. Neuropsychopharmacology, 38, 863–871.CrossRefGoogle ScholarPubMed
Kringelbach, M. L. (2005). The human orbitofrontal cortex: Linking reward to hedonic experience. Nature Review Neuroscience, 6, 691–702.CrossRefGoogle ScholarPubMed
Liu, X., Hairston, J., Schrier, M., & Fan, J. (2011). Common and distinct networks underlying reward valence and processing stages: A meta-analysis of functional neuroimaging studies. Neuroscience and Biobehavioral Review, 35, 1219–1236.CrossRefGoogle ScholarPubMed
Lundorff, M., Holmgren, H., Zachariae, R., Farver-Vestergaard, I., & O'Connor, M. (2017). Prevalence of prolonged grief disorder in adult bereavement: A systematic review and meta-analysis. Journal of Affective Disorders, 212, 138–149.CrossRefGoogle ScholarPubMed
Maccallum, F., & Bryant, R. A. (2008). Self-defining memories in complicated grief. Behaviour Research and Therapy, 46, 1311–1315.CrossRefGoogle ScholarPubMed
Maccallum, F., & Bryant, R. A. (2010). Impaired autobiographical memory in complicated grief. Behaviour Research and Therapy, 48, 328–334.CrossRefGoogle ScholarPubMed
Maccallum, F., & Bryant, R. A. (2013). A cognitive attachment model of prolonged grief: Integrating attachments, memory, and identity. Clinical Psychology Review, 33, 713–727.CrossRefGoogle ScholarPubMed
Maercker, A., Brewin, C. R., Bryant, R. A., Cloitre, M., Reed, G. M., van Ommeren, M., et al. (2013). Proposals for mental disorders specifically associated with stress in the International Classification of Diseases-11. Lancet, 381, 1683–1685.CrossRefGoogle ScholarPubMed
Meerwijk, E. L., Ford, J. M., & Weiss, S. J. (2013). Brain regions associated with psychological pain: Implications for a neural network and its relationship to physical pain. Brain Imaging and Behavior, 7, 1–14.CrossRefGoogle ScholarPubMed
Murphy, F. C., Nimmo-Smith, I., & Lawrence, A. D. (2003). Functional neuroanatomy of emotions: A meta-analysis. Cognitive, Affective, & Behavioral Neuroscience, 3, 207–233.CrossRefGoogle ScholarPubMed
O'Connor, M. F., Wellisch, D. K., Stanton, A. L., Eisenberger, N. I., Irwin, M. R., & Lieberman, M. D. (2008). Craving love? Enduring grief activates brain's reward center. Neuroimage, 42, 969–972.CrossRefGoogle ScholarPubMed
Price, J. L., & Drevets, W. C. (2010). Neurocircuitry of mood disorders. Neuropsychopharmacology, 35, 192–216.CrossRefGoogle ScholarPubMed
Prigerson, H. G., Horowitz, M. J., Jacobs, S. C., Parkes, C. M., Aslan, M., Goodkin, K., et al. (2009). Prolonged grief disorder: Psychometric validation of criteria proposed for DSM-V and ICD-11. PLoS Medicine, 6, e1000121.CrossRefGoogle ScholarPubMed
Prigerson, H. G., & Maciejewski, P. J. (2007) Prolonged grief disorder (PG-13). Boston: Center for Psychooncology & Palliative Care Research.Google Scholar
Robinaugh, D. J., LeBlanc, N. J., Vuletich, H. A., & McNally, R. J. (2014). Network analysis of persistent complex bereavement disorder in conjugally bereaved adults. Journal of Abnormal Psychology, 123, 510–522.CrossRefGoogle ScholarPubMed
Sartor, C. E., Grant, J. D., Lynskey, M. T., McCutcheon, V. V., Waldron, M., Statham, D. J., et al. (2012). Common heritable contributions to low-risk trauma, high-risk trauma, posttraumatic stress disorder, and major depression. Archives of General Psychiatry, 69, 293–299.CrossRefGoogle ScholarPubMed
Shalev, A., Liberzon, I., & Marmar, C. (2017). Post-traumatic stress disorder. New England Journal of Medicine, 376, 2459–2469.CrossRefGoogle ScholarPubMed
Sheehan, D. V., Lecrubier, Y., Harnett-Sheehan, K., Amorim, P., Janavs, J., Weiller, E., et al. (1998). The Mini International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview. Journal of Clinical Psychiatry, 59, 22–33.Google ScholarPubMed
Smith, K. S. & Berridge, K. C. (2005). The ventral pallidum and hedonic reward: Neurochemical maps of sucrose “liking” and food intake. Journal of Neuroscience, 25, 8637–8649.CrossRefGoogle ScholarPubMed
Smith, K. S., Tindell, A. J., Aldridge, J. W., & Berridge, K. C. (2009). Ventral pallidum roles in reward and motivation. Behavioural Brain Research, 196, 155–167.CrossRefGoogle ScholarPubMed
Wager, T. D., Kang, J., Johnson, T. D., Nichols, T. E., Satpute, A. B., & Barrett, L. F. (2015) A Bayesian model of category-specific emotional brain responses. PLoS Computational Biology, 11, e1004066.CrossRefGoogle ScholarPubMed
Wallis, J. D. (2007). Orbitofrontal cortex and its contribution to decision-making. Annual Review of Neuroscience, 30, 31–56.CrossRefGoogle ScholarPubMed
Williams, L. M. (2016). Precision psychiatry: A neural circuit taxonomy for depression and anxiety. The Lancet. Psychiatry, 3, 472–480.CrossRefGoogle ScholarPubMed
Williams, L. M., Das, P., Liddell, B. J., Kemp, A. H., Rennie, C. J., & Gordon, E. (2006). Mode of functional connectivity in amygdala pathways dissociates level of awareness for signals of fear. Journal of Neuroscience, 26, 9264–9271.CrossRefGoogle Scholar
Williams, L. M., Liddell, B. J., Rathjen, J., Brown, K. J., Gray, J., Phillips, M., et al. (2004). Mapping the time course of nonconscious and conscious perception of fear: An integration of central and peripheral measures. Human Brain Mapping, 21, 64–74.CrossRefGoogle ScholarPubMed