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Brain imaging in catatonia: systematic review and directions for future research

Published online by Cambridge University Press:  16 June 2020

Alexandre Haroche Open the ORCID record for Alexandre Haroche [Opens in a new window] ,
Jonathan Rogers ,
Marion Plaze ,
Raphaël Gaillard ,
Steve CR Williams ,
Pierre Thomas  and
Ali Amad
Alexandre Haroche*
Affiliation:
GHU PARIS Psychiatrie & Neurosciences, site Sainte-Anne, Service Hospitalo-Universitaire, Pôle Hospitalo-Universitaire Paris 15, Paris, France
Jonathan Rogers
Affiliation:
Division of Psychiatry, University College London, London, UK South London and Maudsley NHS Foundation Trust, London, UK
Marion Plaze
Affiliation:
GHU PARIS Psychiatrie & Neurosciences, site Sainte-Anne, Service Hospitalo-Universitaire, Pôle Hospitalo-Universitaire Paris 15, Paris, France
Raphaël Gaillard
Affiliation:
GHU PARIS Psychiatrie & Neurosciences, site Sainte-Anne, Service Hospitalo-Universitaire, Pôle Hospitalo-Universitaire Paris 15, Paris, France
Steve CR Williams
Affiliation:
Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK
Pierre Thomas
Affiliation:
Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, F-59000, Lille, France
Ali Amad
Affiliation:
Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, F-59000, Lille, France
*
Author for correspondence: Alexandre Haroche, E-mail: a.haroche@ghu-paris.fr
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Abstract

Background

Catatonia is a frequent, complex and severe identifiable syndrome of motor dysregulation. However, its pathophysiology is poorly understood.

Methods

We aimed to provide a systematic review of all brain imaging studies (both structural and functional) in catatonia.

Results

We identified 137 case reports and 18 group studies representing 186 individual patients with catatonia. Catatonia is often associated with brain imaging abnormalities (in more than 75% of cases). The majority of the case reports show diffuse lesions of white matter, in a wide range of brain regions. Most of the case reports of functional imaging usually show frontal, temporal, or basal ganglia hypoperfusion. These abnormalities appear to be alleviated after successful treatment of clinical symptoms. Structural brain magnetic resonance imaging studies are very scarce in the catatonia literature, mostly showing diffuse cerebral atrophy. Group studies assessing functional brain imaging after catatonic episodes show that emotional dysregulation is related to the GABAergic system, with hypoactivation of orbitofrontal cortex, hyperactivation of median prefrontal cortex, and dysconnectivity between frontal and motor areas.

Conclusion

In catatonia, brain imaging is abnormal in the majority of cases, and abnormalities more frequently diffuse than localised. Brain imaging studies published so far suffer from serious limitations and for now the different models presented in the literature do not explain most of the cases. There is an important need for further studies including a better clinical characterisation of patients with catatonia, functional imaging with concurrent catatonic symptoms and the use of novel brain imaging techniques.

Keywords

Bipolar disorderbrain imagingcatatonia
Type
Review Article
Information
Psychological Medicine , Volume 50 , Issue 10 , July 2020 , pp. 1585 - 1597
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

American Psychiatric Association, American Psychiatric Association, DSM-5 Task Force (2013). Diagnostic and statistical manual of mental disorders: DSM-5. Arlington, VA: American Psychiatric Association.Google Scholar
Baruk, H., & de Jong, H. (1930). La catatonie expérimentale par la bulbocapnine. Paris: Masson.Google Scholar
Bearden, C. E., & Monterosso, J. R. (2002). Catatonia isn't ready for a unified theory. Behavioral and Brain Sciences, 25, 579–580.CrossRefGoogle Scholar
Carroll, B. T. (2000). The universal field hypothesis of catatonia and neuroleptic malignant syndrome. CNS Spectrums, 5, 26–33.CrossRefGoogle ScholarPubMed
Dao-Castellana, M. H., Paillère-Martinot, M. L., Hantraye, P., Attar-Lévy, D., Rémy, P., Crouzel, C., … Martinot, J. L. (1997). Presynaptic dopaminergic function in the striatum of schizophrenic patients. Schizophrenia Research, 23, 167–174.CrossRefGoogle ScholarPubMed
Dziadziuszko, K., Szurowska, E., Pienkowska, J., Jassem, J., & Dziadziuszko, R. (2014). Miliary brain metastases in a patient with ROS1-rearranged lung adenocarcinoma: A case report. Journal of Thoracic Oncology, 9, e34–e36.CrossRefGoogle Scholar
Escobar, R., Rios, A., Montoya, I. D., Lopera, F., Ramos, D., Carvajal, C., … Herrera, C. P. (2000). Clinical and cerebral blood flow changes in catatonic patients treated with ECT. Journal of psychosomatic research, 49, 423–429.CrossRefGoogle ScholarPubMed
Fink, M. (2013). Rediscovering catatonia: The biography of a treatable syndrome. Acta Psychiatrica Scandinavica, 127, 1–47.CrossRefGoogle Scholar
Fink, M., & Taylor, M. A. (2006). Catatonia: A clinician's guide to diagnosis and treatment. Cambridge: Cambridge University Press.Google Scholar
Foucher, J. R., Zhang, Y. F., Roser, M., Lamy, J., De Sousa, P. L., Weibel, S., … Berna, F. (2018). A double dissociation between two psychotic phenotypes: Periodic catatonia and cataphasia. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 86, 363–369.CrossRefGoogle ScholarPubMed
Fricchione, G., Mann, S. C., & Caroff, S. N. (2000). Catatonia, lethal catatonia, and neuroleptic malignant syndrome. Psychiatric Annals, 30, 347–355.CrossRefGoogle Scholar
Hietala, J., Syvälahti, E., Vilkman, H., Vuorio, K., Räkköläinen, V., Bergman, J., … Salokangas, R. K. (1999). Depressive symptoms and presynaptic dopamine function in neuroleptic-naive schizophrenia. Schizophrenia Research, 35, 41–50.CrossRefGoogle ScholarPubMed
Hietala, J., Syvälahti, E., Vuorio, K., Räkköläinen, V., Bergman, J., Haaparanta, M., … Ruotsalainen, U. (1995). Presynaptic dopamine function in striatum of neuroleptic-naive schizophrenic patients. Lancet (London, England), 346, 1130–1131.CrossRefGoogle ScholarPubMed
Hirjak, D., Kubera, K. M., Northoff, G., Fritze, S., Bertolino, A. L., Topor, C. E., … Wolf, R. C. (2019 a). Cortical contributions to distinct symptom dimensions of catatonia. Schizophrenia bulletin, 45(6), 1184–1194.CrossRefGoogle ScholarPubMed
Hirjak, D., Kubera, K. M., Wolf, R. C., & Northoff, G. (2019 b). Going back to Kahlbaum's Psychomotor (and GABAergic) origins: Is catatonia more than just a motor and dopaminergic syndrome? Schizophrenia bulletin, 46(2), 272–285.Google Scholar
Hirjak, D., Rashidi, M., Kubera, K. M., Northoff, G., Fritze, S., Schmitgen, M. M., … Wolf, R. C. (2019 c). Multimodal magnetic resonance imaging data fusion reveals distinct patterns of abnormal brain structure and function in catatonia. Schizophrenia Bulletin, 46(1), 202–210.CrossRefGoogle Scholar
Joseph, R. (1999). Frontal lobe psychopathology: Mania, depression, confabulation, catatonia, perseveration, obsessive compulsions, and schizophrenia. Psychiatry, 62, 138–172.CrossRefGoogle Scholar
Joseph, A. B., Anderson, W. H., & O'Leary, D. H. (1985). Brainstem and vermis atrophy in catatonia. The American Journal of Psychiatry, 142, 352–354.Google ScholarPubMed
Kahlbaum, K. L. (1874). Die Katatonie: oder das Spannungsirresein, eine klinische Form psychischer Krankheit. Berlin: Hirschwald.Google Scholar
Lauer, M., Schirrmeister, H., Gerhard, A., Ellitok, E., Beckmann, H., Reske, S. N., & Stöber, G. (2001). Disturbed neural circuits in a subtype of chronic catatonic schizophrenia demonstrated by F-18-FDG-PET and F-18-DOPA-PET. Journal of Neural Transmission (Vienna, Austria: 1996), 108, 661–670.CrossRefGoogle Scholar
Liddle, P. F., Friston, K. J., Frith, C. D., Hirsch, S. R., Jones, T., & Frackowiak, R. S. J. (1992). Patterns of cerebral blood flow in schizophrenia. The British Journal of Psychiatry, 160, 179–186.CrossRefGoogle Scholar
Medda, P., Toni, C., Luchini, F., Giorgi Mariani, M., Mauri, M., & Perugi, G. (2015). Catatonia in 26 patients with bipolar disorder: Clinical features and response to electroconvulsive therapy. Bipolar Disorders, 17, 892–901.CrossRefGoogle ScholarPubMed
Nguyen Thi Hoang, M., Nguyen Hoan, P., Le Van, T., McBride, A., Ho Dang Trung, N., Tran Tan, T., … Thwaites, G. (2017). First reported cases of anti-NMDA receptor encephalitis in Vietnamese adolescents and adults. Journal of the Neurological Sciences, 373, 250–253.CrossRefGoogle ScholarPubMed
Northoff, G. (2000). Brain imaging in catatonia: Current findings and a pathophysiologic model. CNS spectrums, 5, 34–46.CrossRefGoogle Scholar
Northoff, G. (2002 a). Catatonia and neuroleptic malignant syndrome: Psychopathology and pathophysiology. Journal of Neural Transmission, 109, 1453–1467.CrossRefGoogle ScholarPubMed
Northoff, G. (2002 b). What catatonia can tell us about ‘top-down modulation’: A neuropsychiatric hypothesis. Behavioral and Brain Sciences, 25, 555–577.CrossRefGoogle Scholar
Northoff, G., Braus, D. F., Sartorius, A., Khoram-Sefat, D., Russ, M., Eckert, J., … Henn, F. A. (1999 a). Reduced activation and altered laterality in two neuroleptic-naive catatonic patients during a motor task in functional MRI. Psychological Medicine, 29, 997–1002.CrossRefGoogle ScholarPubMed
Northoff, G., Koch, A., Wenke, J., Eckert, J., Böker, H., Pflug, B., & Bogerts, B. (1999 b). Catatonia as a psychomotor syndrome: A rating scale and extrapyramidal motor symptoms. Movement Disorders: Official Journal of the Movement Disorder Society, 14, 404–416.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Northoff, G., Kötter, R., Baumgart, F., Danos, P., Boeker, H., Kaulisch, T., … Bogerts, B. (2004). Orbitofrontal cortical dysfunction in akinetic catatonia: A functional magnetic resonance imaging study during negative emotional stimulation. Schizophrenia Bulletin, 30, 405.CrossRefGoogle ScholarPubMed
Northoff, G., Steinke, R., Czcervenka, C., Krause, R., Ulrich, S., Danos, P., … Bogerts, B. (1999 c). Decreased density of GABA-A receptors in the left sensorimotor cortex in akinetic catatonia: Investigation of in vivo benzodiazepine receptor binding. Journal of Neurology Neurosurgery & Psychiatry, 67, 445–450.CrossRefGoogle ScholarPubMed
Northoff, G., Steinke, R., Nagel, D., Czerwenka, C., Grosser, O., Danos, P., … (2000). Right lower prefronto-parietal cortical dysfunction in akinetic catatonia: A combined study of neuropsychology and regional cerebral blood flow. Psychological Medicine, 30, 583–596.CrossRefGoogle ScholarPubMed
Northoff, G., Waters, H., Mooren, I., Schlüter, U., Diekmann, S., Falkai, P., & Bogerts, B. (1999 d). Cortical sulcal enlargement in catatonic schizophrenia: A planimetric CT study. Psychiatry Research: Neuroimaging, 91, 45–54.CrossRefGoogle ScholarPubMed
Richter, A., Grimm, S., & Northoff, G. (2010). Lorazepam modulates orbitofrontal signal changes during emotional processing in catatonia. Human Psychopharmacology: Clinical and Experimental, 25, 55–62.CrossRefGoogle ScholarPubMed
Rogers, J. P., Pollak, T. A., Blackman, G., & David, A. S. (2019). Catatonia and the immune system: A review. The Lancet Psychiatry, 6(7), 620–630.CrossRefGoogle ScholarPubMed
Sarkar, S., Sakey, S., Mathan, K., Bharadwaj, B., Kattimani, S., & Rajkumar, R. P. (2016). Assessing catatonia using four different instruments: Inter-rater reliability and prevalence in inpatient clinical population. Asian Journal of Psychiatry, 23, 27–31.CrossRefGoogle ScholarPubMed
Satoh, K., Suzuki, T., Narita, M., Ishikura, S., Shibasaki, M., Kato, T., … Morita, R. (1993). Regional cerebral blood flow in catatonic schizophrenia. Psychiatry Research: Neuroimaging, 50, 203–216.CrossRefGoogle ScholarPubMed
Scheuerecker, J., Ufer, S., Käpernick, M., Wiesmann, M., Brückmann, H., Kraft, E., … Meisenzahl, E. M. (2009). Cerebral network deficits in post-acute catatonic schizophrenic patients measured by fMRI. Journal of Psychiatric Research, 43, 607–614.CrossRefGoogle ScholarPubMed
Shioiri, T., Someya, T., Murashita, J., Kato, T., Hamakawa, H., Fujii, K., & Inubushi, T. (1997). Multiple regression analysis of relationship between frontal lobe phosphorus metabolism and clinical symptoms in patients with schizophrenia. Psychiatry Research: Neuroimaging, 76, 113–122.CrossRefGoogle ScholarPubMed
Smith, J. H., Smith, V. D., Philbrick, K. L., & Kumar, N. (2012). Catatonic disorder due to a general medical or psychiatric condition. The Journal of Neuropsychiatry and Clinical Neurosciences, 24, 198–207.CrossRefGoogle ScholarPubMed
Solmi, M., Pigato, G. G., Roiter, B., Guaglianone, A., Martini, L., Fornaro, M., … Correll, C. U. (2018). Prevalence of Catatonia and its moderators in clinical samples: Results from a meta-analysis and meta-regression analysis. Schizophrenia Bulletin, 44, 1133–1150.CrossRefGoogle ScholarPubMed
Vancaester, E., & Santens, P. (2007). Catatonia and neuroleptic malignant syndrome: Two sides of a coin? Acta Neurologica Belgica, 107, 47.Google ScholarPubMed
Walther, S., Schäppi, L., Federspiel, A., Bohlhalter, S., Wiest, R., Strik, W., & Stegmayer, K. (2016). Resting-State hyperperfusion of the supplementary motor area in Catatonia. Schizophrenia Bulletin, 43(5), 972–981. sbw140.Google Scholar
Walther, S.,Stegmayer, K., Federspiel, A., Bohlhalter, S., Wiest, R., & Viher, P. (2017). Aberrant hyperconnectivity in the motor system at rest is linked to motor abnormalities in schizophrenia spectrum disorders. Schizophrenia Bulletin, 43(5), 982–992.CrossRefGoogle ScholarPubMed
Walther, S., Stegmayer, K., Wilson, J. E., & Heckers, S. (2019). Structure and neural mechanisms of catatonia. The Lancet Psychiatry, 6(7), 610–619.CrossRefGoogle ScholarPubMed
Walther, S., & Strik, W. (2016). Catatonia. CNS Spectrums, 21, 341–348.CrossRefGoogle ScholarPubMed
Wilcox, J. A. (1991). Cerebellar atrophy and catatonia. Biological Psychiatry, 29, 733–734.CrossRefGoogle ScholarPubMed
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