Anosognosia and default mode subnetwork dysfunction in Alzheimer's disease

[en] Research on the neural correlates of anosognosia in Alzheimer's disease varied according to methods and objectives: they compared different measures, used diverse neuroimaging modalities, explored connectivity between brain networks, addressed the role of specific brain regions or tried to give support to theoretical models of unawareness. We used resting-state fMRI connectivity with two different seed regions and two measures of anosognosia in different patient samples to investigate consistent modifications of default mode subnetworks and we aligned the results with the Cognitive Awareness Model. In a first study, patients and their relatives were presented with the Memory Awareness Rating Scale. Anosognosia was measured as a patient-relative discrepancy score and connectivity was investigated with a parahippocampal seed. In a second study, anosognosia was measured in patients with brain amyloid (taken as a disease biomarker) by comparing self-reported rating with memory performance, and connectivity was examined with a hippocampal seed. In both studies, anosognosia was consistently related to disconnection within the medial temporal subsystem of the default mode network, subserving episodic memory processes. Importantly, scores were also related to disconnection between the medial temporal and both the core subsystem (participating to self-reflection) and the dorsomedial subsystem of the default mode network (the middle temporal gyrus that might subserve a personal database in the second study). We suggest that disparity in connectivity within and between subsystems of the default mode network may reflect impaired functioning of pathways in cognitive models of awareness. © 2019 The Authors. Human Brain Mapping published by Wiley Periodicals, Inc.

Research Center/Unit :

GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège

Disciplines :

Neurology

Author, co-author :

Antoine, Nicolas ; Université de Liège - ULiège > Doct. sc. médicales (Bologne)

Bahri, Mohamed Ali ; Université de Liège - ULiège > CRC In vivo Imaging-Aging & Memory

Bastin, Christine ; Université de Liège - ULiège > CRC In vivo Imaging-Aging & Memory

Collette, Fabienne ; Université de Liège - ULiège > Département de Psychologie > Neuropsychologie

Phillips, Christophe ; Université de Liège - ULiège > CRC In vivo Im.-Neuroimaging, data acquisition & processing

Balteau, Evelyne ; Université de Liège - ULiège > CRC In vivo Im.-Neuroimaging, data acquisition & processing

Genon, Sarah ; Université de Liège - ULiège > CRC In vivo Imaging-Aging & Memory

Salmon, Eric ; Université de Liège - ULiège > Département des sciences cliniques > Neuroimagerie des troubles de la mémoire et revalid. cogn.

Language :

English

Title :

Anosognosia and default mode subnetwork dysfunction in Alzheimer's disease

Publication date :

2019

Journal title :

Human Brain Mapping

ISSN :

1065-9471

eISSN :

1097-0193

Publisher :

John Wiley and Sons Inc.

Volume :

Pages :

5330-5340

Peer reviewed :

Peer Reviewed verified by ORBi

Name of the research project :

DFG: GE 2835/1‐1; DFG12/17‐01

Funders :

DFG - Deutsche Forschungsgemeinschaft
FRB - Fondation Roi Baudouin

Available on ORBi :

since 19 December 2019

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Bibliography

Addis, D. R., Wong, A. T., & Schacter, D. L. (2007). Remembering the past and imagining the future: Common and distinct neural substrates during event construction and elaboration. Neuropsychologia, 45, 1363–1377.
Agnew, S. K., & Morris, R. G. (1998). The heterogeneity of anosognosia for memory impairment in Alzheimer's disease: A review of the literature and a proposed model. Aging & Mental Health, 2, 7–19.
Andrews-Hanna, J. R., Reidler, J. S., Sepulcre, J., Poulin, R., & Buckner, R. L. (2010). Functional-anatomic fractionation of the brain's default network. Neuron, 65, 550–562.
Berlingeri, M., Ravasio, A., Cranna, S., Basilico, S., Sberna, M., Bottini, G., & Paulesu, E. (2015). Unrealistic representations of "the self": A cognitive neuroscience assessment of anosognosia for memory deficit. Consciousness and Cognition, 37, 160–177.
Berryhill, M. E., Phuong, L., Picasso, L., Cabeza, R., & Olson, I. R. (2007). Parietal lobe and episodic memory: Bilateral damage causes impaired free recall of autobiographical memory. The Journal of Neuroscience, 27, 14415–14423.
Binder, J. R., & Desai, R. H. (2011). The neurobiology of semantic memory. Trends in Cognitive Sciences, 15, 527–536.
Bird, C. M., Keidel, J. L., Ing, L. P., Horner, A. J., & Burgess, N. (2015). Consolidation of complex events via reinstatement in posterior cingulate cortex. The Journal of Neuroscience, 35, 14426–14434.
Byrne, P., Becker, S., & Burgess, N. (2007). Remembering the past and imagining the future: A neural model of spatial memory and imagery. Psychological Review, 114, 340–375.
Chavoix, C., & Insausti, R. (2017). Self-awareness and the medial temporal lobe in neurodegenerative diseases. Neuroscience and Biobehavioral Reviews, 78, 1–12.
Clare, L., Markova, I., Verhey, F., & Kenny, G. (2005). Awareness in dementia: A review of assessment methods and measures. Aging & Mental Health, 9, 394–413.
Clare, L., Markova, I. S., Roth, I., & Morris, R. G. (2011). Awareness in Alzheimer's disease and associated dementias: Theoretical framework and clinical implications. Aging & Mental Health, 15, 936–944.
Clare, L., Whitaker, C. J., & Nelis, S. M. (2010). Appraisal of memory functioning and memory performance in healthy ageing and early-stage Alzheimer's disease. Neuropsychology, Development, and Cognition. Section B, Aging, Neuropsychology and Cognition, 17, 462–491.
Clare, L., Wilson, B. A., Carter, G., Roth, I., & Hodges, J. R. (2002). Assessing awareness in early-stage Alzheimer's disease: Development and piloting of the memory awareness rating scale. Neuropsychological Rehabilitation, 12, 341–362.
D'Argembeau, A., Cassol, H., Phillips, C., Balteau, E., Salmon, E., & Van der Linden, M. (2014). Brains creating stories of selves: The neural basis of autobiographical reasoning. Social Cognitive and Affective Neuroscience, 9, 646–652.
Deichmann, R., Schwarzbauer, C., & Turner, R. (2004). Optimisation of the 3D MDEFT sequence for anatomical brain imaging: Technical implications at 1.5 and 3 T. NeuroImage, 21, 757–767.
Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). "mini-mental state". A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.
Galeone, F., Pappalardo, S., Chieffi, S., Iavarone, A., & Carlomagno, S. (2011). Anosognosia for memory deficit in amnestic mild cognitive impairment and Alzheimer's disease. International Journal of Geriatric Psychiatry, 26, 695–701.
Genon, S., & Salmon, E. (2018). Disrupted self in Alzheimer's disease: Beyond midline structures: Commentary on Wong et al. Cortex, 104, 128–129.
Gerretsen, P., Chung, J. K., Shah, P., Plitman, E., Iwata, Y., Caravaggio, F., … for the Alzheimer's Disease Neuroimaging Initiative. (2017). Anosognosia is an independent predictor of conversion from mild cognitive impairment to Alzheimer's disease and is associated with reduced brain metabolism. The Journal of Clinical Psychiatry, 78, e1187–e1196.
Kahn, I., Andrews-Hanna, J. R., Vincent, J. L., Snyder, A. Z., & Buckner, R. L. (2008). Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity. Journal of Neurophysiology, 100, 129–139.
Kurth, S., Moyse, E., Bahri, M. A., Salmon, E., & Bastin, C. (2015). Recognition of personally familiar faces and functional connectivity in Alzheimer's disease. Cortex, 67, 59–73.
Lawton, M. P., & Brody, E. M. (1969). Assessment of older people: Self-maintaining and instrumental activities of daily living. Gerontologist, 9, 179–186.
Leech, R., & Sharp, D. J. (2014). The role of the posterior cingulate cortex in cognition and disease. Brain, 137, 12–32.
Martinelli, P., Anssens, A., Sperduti, M., & Piolino, P. (2013). The influence of normal aging and Alzheimer's disease in autobiographical memory highly related to the self. Neuropsychology, 27, 69–78.
Mattis, S. (1976). Mental status examination for organic mental syndrome in the elderly patients. In L. Bellack & B. Karasu (Eds.), Geriatric psychiatry (pp. 77–121). New York: Grune & Stratton.
McGlynn, S. M., & Schacter, D. L. (1989). Unawareness of deficits in neuropsychological syndromes. Journal of Clinical and Experimental Neuropsychology, 11, 143–205.
McKhann, G. M., Knopman, D. S., Chertkow, H., Hyman, B. T., Jack, C. R., Jr., Kawas, C. H., … Phelps, C. H. (2011). The diagnosis of dementia due to Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement, 7, 263–269.
Mimura, M., & Yano, M. (2006). Memory impairment and awareness of memory deficits in early-stage Alzheimer's disease. Reviews in the Neurosciences, 17, 253–266.
Morris, J. C. (1993). The clinical dementia rating (CDR): Current version and scoring rules. Neurology, 43, 2412–2414.
Morris, R. G., & Mograbi, D. C. (2013). Anosognosia, autobiographical memory and self knowledge in Alzheimer's disease. Cortex, 49, 1553–1565.
Nelissen, N., Van Laere, K., Thurfjell, L., Owenius, R., Vandenbulcke, M., Koole, M., … Vandenberghe, R. (2009). Phase 1 study of the Pittsburgh compound B derivative 18F-flutemetamol in healthy volunteers and patients with probable Alzheimer disease. Journal of Nuclear Medicine, 50, 1251–1259.
Northoff, G., Heinzel, A., de Greck, M., Bermpohl, F., Dobrowolny, H., & Panksepp, J. (2006). Self-referential processing in our brain–a meta-analysis of imaging studies on the self. NeuroImage, 31, 440–457.
Perrotin, A., Desgranges, B., Landeau, B., Mezenge, F., La Joie, R., Egret, S., … Chetelat, G. (2015). Anosognosia in Alzheimer disease: Disconnection between memory and self-related brain networks. Annals of Neurology, 78, 477–486.
Rey, A. (1964). L'examen clinique en psychologie. Paris: Presse Universitaires de France.
Ries, M. L., McLaren, D. G., Bendlin, B. B., Xu, G., Rowley, H. A., Birn, R., … Johnson, S. C. (2012). Medial prefrontal functional connectivity–Relation to memory self-appraisal accuracy in older adults with and without memory disorders. Neuropsychologia, 50, 603–611.
Rosen, H. J. (2011). Anosognosia in neurodegenerative disease. Neurocase, 17, 231–241.
Rosen, H. J., Alcantar, O., Rothlind, J., Sturm, V., Kramer, J. H., Weiner, M., & Miller, B. L. (2010). Neuroanatomical correlates of cognitive self-appraisal in neurodegenerative disease. NeuroImage, 49, 3358–3364.
Ruby, P., Collette, F., D'Argembeau, A., Peters, F., Degueldre, C., Balteau, E., … Salmon, E. (2009). Perspective taking to assess self-personality: what's modified in Alzheimer's disease? Neurobiology of Aging, 30, 1637–1651.
Rugg, M. D., & King, D. R. (2018). Ventral lateral parietal cortex and episodic memory retrieval. Cortex, 107, 238–250.
Salmon, E., Perani, D., Herholz, K., Marique, P., Kalbe, E., Holthoff, V., … Garraux, G. (2006). Neural correlates of anosognosia for cognitive impairment in Alzheimer's disease. Human Brain Mapping, 27, 588–597.
Schachter, D. L. (1991). Unawareness of deficit and unawareness of knowledge in patients with memory disorders. In G. P. Prigatano & D. L. Schachter (Eds.), Awareness of deficit after brain injury: Clinical and theoretical issues (pp. 127–151). New York, NY, US: Oxford University Press.
Scheltens, P., Leys, D., Barkhof, F., Huglo, D., Weinstein, H. C., Vermersch, P., … Valk, J. (1992). Atrophy of medial temporal lobes on MRI in "probable" Alzheimer's disease and normal ageing: Diagnostic value and neuropsychological correlates. Journal of Neurology, Neurosurgery, and Psychiatry, 55, 967–972.
Sha, Z., Wager, T. D., Mechelli, A., & He, Y. (2019). Common dysfunction of large-scale neurocognitive networks across psychiatric disorders. Biological Psychiatry, 85, 379–388.
Starkstein, S. E. (2014). Anosognosia in Alzheimer's disease: Diagnosis, frequency, mechanism and clinical correlates. Cortex, 61, 64–73.
Sunderaraman, P., & Cosentino, S. (2017). Integrating the constructs of Anosognosia and metacognition: A review of recent findings in dementia. Current Neurology and Neuroscience Reports, 17, 27.
Svoboda, E., McKinnon, M. C., & Levine, B. (2006). The functional neuroanatomy of autobiographical memory: A meta-analysis. Neuropsychologia, 44, 2189–2208.
Therriault, J., Ng, K. P., Pascoal, T. A., Mathotaarachchi, S., Kang, M. S., Struyfs, H., … For the Alzheimer's Disease Neuroimaging Initiative. (2018). Anosognosia predicts default mode network hypometabolism and clinical progression to dementia. Neurology, 90, e932–e939.
Thurfjell, L., Lilja, J., Lundqvist, R., Buckley, C., Smith, A., Vandenberghe, R., & Sherwin, P. (2014). Automated quantification of 18F-flutemetamol PET activity for categorizing scans as negative or positive for brain amyloid: Concordance with visual image reads. Journal of Nuclear Medicine, 55, 1623–1628.
Tondelli, M., Barbarulo, A. M., Vinceti, G., Vincenzi, C., Chiari, A., Nichelli, P. F., & Zamboni, G. (2018). Neural correlates of Anosognosia in Alzheimer's disease and mild cognitive impairment: A multi-method assessment. Frontiers in Behavioral Neuroscience, 12, 100.
Tulving, E. (2002). Episodic memory: From mind to brain. Annual Review of Psychology, 53, 1–25.
Vann, S. D., Aggleton, J. P., & Maguire, E. A. (2009). What does the retrosplenial cortex do? Nature Reviews. Neuroscience, 10, 792–802.
Vannini, P., Hanseeuw, B., Munro, C. E., Amariglio, R. E., Marshall, G. A., Rentz, D. M., … Sperling, R. A. (2017). Anosognosia for memory deficits in mild cognitive impairment: Insight into the neural mechanism using functional and molecular imaging. Neuroimage Clin, 15, 408–414.
Vilberg, K. L., & Rugg, M. D. (2008). Memory retrieval and the parietal cortex: A review of evidence from a dual-process perspective. Neuropsychologia, 46, 1787–1799.
Vogt, B. A., Vogt, L., & Laureys, S. (2006). Cytology and functionally correlated circuits of human posterior cingulate areas. NeuroImage, 29, 452–466.
Wagner, A. D., Shannon, B. J., Kahn, I., & Buckner, R. L. (2005). Parietal lobe contributions to episodic memory retrieval. Trends in Cognitive Sciences, 9, 445–453.
Weiler, M., Northoff, G., Damasceno, B. P., & Balthazar, M. L. F. (2016). Self, cortical midline structures and the resting state: Implications for Alzheimer's disease. Neuroscience and Biobehavioral Reviews, 68, 245–255.
Whitfield-Gabrieli, S., & Nieto-Castanon, A. (2012). Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connectivity, 2, 125–141.
Wilson, B. A., Cockburn, J., & Baddeley, A. D. (1985). The Rivermead behavioural memory test. Bury St Edmunds, UK: Thames Valley Test Company.
Winblad, B., Palmer, K., Kivipelto, M., Jelic, V., Fratiglioni, L., Wahlund, L. O., … Petersen, R. C. (2004). Mild cognitive impairment–beyond controversies, towards a consensus: Report of the international working group on mild cognitive impairment. Journal of Internal Medicine, 256, 240–246.
Zamboni, G., & Wilcock, G. (2011). Lack of awareness of symptoms in people with dementia: The structural and functional basis. International Journal of Geriatric Psychiatry, 26, 783–792.
Zigmond, A. S., & Snaith, R. P. (1983). The hospital anxiety and depression scale. Acta Psychiatrica Scandinavica, 67, 361–370.