Abstract
Posterior cortical atrophy (PCA) is a rare neurodegenerative condition characterized by progressive visual and visuospatial dysfunction. The consensus criteria state that patients should present “relatively spared behavior and personality” in early stages. However, limited research has focused on these symptoms in PCA. This study compared 157 patients with PCA in early stages of the disease with 352 healthy controls (HC), 202 typical AD (tAD), and 177 logopenic variant primary progressive aphasia (lvPPA) patients from the National Alzheimer's Coordinating Center (NACC) dataset. They were compared using clinician ratings of behavioral symptoms, informant- and clinician-filled questionnaires and patient-facing tests of behavior and social cognition. Results showed that PCA individuals exhibited many behavioral symptoms, the more frequently reported being anxiety, depression, apathy, and irritability. During cognitive testing, clinicians observed disorganized and reactive behaviors, but no insensitive behaviors. Informant reports indicated that PCA patients exhibited higher levels of inhibition and anxiety in response to stimuli associated with non-reward, novelty, and punishment. Social norms knowledge and empathy were overall preserved, although slight decreases in perspective-taking and socioemotional sensitivity were observed on informant-rated questionnaires. Except for more elevated neuropsychiatric symptoms in tAD, the three AD variants had similar profiles. Our findings provide insights into the social cognition and behavioral profiles of PCA, highlighting patterns of preservations and mild impairments, even in the early stages of the disease. These results contribute to a more complete understanding of non-visual symptoms in PCA and have implications for diagnostic and intervention strategies.
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Data availability
The data used in this study is from the National Alzheimer’s Coordinating Center (NACC). Data request can be made at https://naccdata.org/.
References
Crutch SJ, Schott JM, Rabinovici GD et al (2017) Consensus classification of posterior cortical atrophy. Alzheimers Dement 13:870–884. https://doi.org/10.1016/j.jalz.2017.01.014
Montembeault M, Lacomblez L, Habert M-O et al (2018) L’atrophie corticale postérieure: de la vision à l’émotion. Gériatrie Psychol Neuropsychiatr Vieil 16:57–66. https://doi.org/10.1684/pnv.2017.0717
Putcha D, McGinnis SM, Brickhouse M et al (2018) Executive dysfunction contributes to verbal encoding and retrieval deficits in posterior cortical atrophy. Cortex 106:36–46. https://doi.org/10.1016/j.cortex.2018.04.010
Trotta L, Lamoureux D, Bartolomeo P, Migliaccio R (2019) Working memory in posterior cortical atrophy. Neurol Sci 40:1713–1716. https://doi.org/10.1007/s10072-019-03869-5
Ahmed S, Baker I, Husain M et al (2016) Memory impairment at initial clinical presentation in posterior cortical atrophy. J Alzheimers Dis 52:1245–1250. https://doi.org/10.3233/JAD-160018
Crutch SJ, Lehmann M, Warren JD, Rohrer JD (2013) The language profile of posterior cortical atrophy. J Neurol Neurosurg Psychiatry 84:460–466. https://doi.org/10.1136/jnnp-2012-303309
Cerejeira J, Lagarto L, Mukaetova-Ladinska E (2012) Behavioral and psychological symptoms of dementia. Front Neurol 3:73
Etchepare A, Prouteau A (2018) Toward a two-dimensional model of social cognition in clinical neuropsychology: a systematic review of factor structure studies. J Int Neuropsychol Soc 24:391–404. https://doi.org/10.1017/S1355617717001163
Rankin KP (2021) Measuring behavior and social cognition in FTLD. Adv Exp Med Biol 1281:51–65. https://doi.org/10.1007/978-3-030-51140-1_4
Beaudoin C, Beauchamp MH (2020) Chapter 21 - Social cognition. In: Gallagher A, Bulteau C, Cohen D, Michaud JL (eds) Handbook of clinical neurology. Elsevier, pp 255–264
Rascovsky K, Hodges JR, Knopman D et al (2011) Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 134:2456–2477. https://doi.org/10.1093/brain/awr179
Younes K, Borghesani V, Montembeault M et al (2022) Right temporal degeneration and socioemotional semantics: semantic behavioural variant frontotemporal dementia. Brain 145:4080–4096. https://doi.org/10.1093/brain/awac217
Fittipaldi S, Ibanez A, Baez S et al (2019) More than words: Social cognition across variants of primary progressive aphasia. Neurosci Biobehav Rev 100:263–284. https://doi.org/10.1016/j.neubiorev.2019.02.020
Christidi F, Migliaccio R, Santamaría-García H et al (2018) Social cognition dysfunctions in neurodegenerative diseases: neuroanatomical correlates and clinical implications. Behav Neurol 2018:1849794. https://doi.org/10.1155/2018/1849794
Setién-Suero E, Murillo-García N, Sevilla-Ramos M et al (2022) Exploring the relationship between deficits in social cognition and neurodegenerative dementia: a systematic review. Front Aging Neurosci 14:778093
Isella V, Villa G, Mapelli C et al (2015) The neuropsychiatric profile of posterior cortical atrophy. J Geriatr Psychiatry Neurol 28:136–144. https://doi.org/10.1177/0891988714554713
Pressman PS, Gola K, Shdo SM et al (2019) Relative preservation of facial expression recognition in posterior cortical atrophy. Neurology 92:e1064–e1071. https://doi.org/10.1212/WNL.0000000000007075
Gonzalez-Gadea ML, Ibanez A, Damm J et al (2015) Different levels of implicit emotional recognition in posterior cortical atrophy (PCA). Neurocase 21:457–464. https://doi.org/10.1080/13554794.2014.919325
Whitwell JL, Martin PR, Graff-Radford J et al (2022) Investigating heterogeneity and neuroanatomic correlates of longitudinal clinical decline in atypical Alzheimer disease. Neurology 98:e2436–e2445. https://doi.org/10.1212/WNL.0000000000200336
Njomboro P (2017) Social cognition deficits: current position and future directions for neuropsychological interventions in cerebrovascular disease. Behav Neurol 2017:e2627487. https://doi.org/10.1155/2017/2627487
McKhann GM, Knopman DS, Chertkow H et al (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 J Alzheimers Assoc 7:263–269. https://doi.org/10.1016/j.jalz.2011.03.005
Gorno-Tempini ML, Hillis AE, Weintraub S et al (2011) Classification of primary progressive aphasia and its variants. Neurology 76:1006–1014. https://doi.org/10.1212/WNL.0b013e31821103e6
Gefen T, Teylan MA, Besser L et al (2020) Measurement and characterization of distinctive clinical phenotypes using the frontotemporal lobar degeneration module (FTLD-MOD). Alzheimers Dement J Alzheimers Assoc 16:918–925. https://doi.org/10.1002/alz.12098
Rankin KP, Kramer JH, Miller BL (2005) Patterns of cognitive and emotional empathy in frontotemporal lobar degeneration. Cogn Behav Neurol Off J Soc Behav Cogn Neurol 18:28–36. https://doi.org/10.1097/01.wnn.0000152225.05377.ab
Rankin KP, Gorno-Tempini ML, Allison SC et al (2006) Structural anatomy of empathy in neurodegenerative disease. Brain J Neurol 129:2945–2956. https://doi.org/10.1093/brain/awl254
Toller G, Ranasinghe K, Cobigo Y et al (2020) Revised self-monitoring scale. Neurology 94:e2384–e2395. https://doi.org/10.1212/WNL.0000000000009451
Carver CS, White TL (1994) Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS Scales. J Pers Soc Psychol 67:319–333. https://doi.org/10.1037/0022-3514.67.2.319
Rankin KP, Toller G, Gavron L et al (2021) Social behavior observer checklist: patterns of spontaneous behaviors differentiate patients with neurodegenerative disease from healthy older adults. Front Neurol 12:683162. https://doi.org/10.3389/fneur.2021.683162
Davis MH (1983) Measuring individual differences in empathy: evidence for a multidimensional approach. J Pers Soc Psychol 44:113–126. https://doi.org/10.1037/0022-3514.44.1.113
Lennox RD, Wolfe RN (1984) Revision of the self-monitoring scale. J Pers Soc Psychol 46:1349–1364. https://doi.org/10.1037/0022-3514.46.6.1349
Toller G, Brown J, Sollberger M et al (2018) Individual differences in socioemotional sensitivity are an index of salience network function. Cortex 103:211–223. https://doi.org/10.1016/j.cortex.2018.02.012
Kramer JH, Mungas D, Possin KL et al (2014) NIH EXAMINER: conceptualization and development of an executive function battery. J Int Neuropsychol Soc 20:11–19. https://doi.org/10.1017/S1355617713001094
Suárez-González A, Crutch SJ, Franco-Macías E, Gil-Néciga E (2016) Neuropsychiatric symptoms in posterior cortical atrophy and Alzheimer disease. J Geriatr Psychiatry Neurol 29:65–71. https://doi.org/10.1177/0891988715606229
Migliaccio R, Agosta F, Rascovsky K et al (2009) Clinical syndromes associated with posterior atrophy: early age at onset AD spectrum. Neurology 73:1571–1578. https://doi.org/10.1212/WNL.0b013e3181c0d427
Chow TE, Veziris CR, La Joie R et al (2023) Increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid-β burden. NeuroImage Clin 37:103282. https://doi.org/10.1016/j.nicl.2022.103282
Fredericks CA, Sturm VE, Brown JA et al (2018) Early affective changes and increased connectivity in preclinical Alzheimer’s disease. Alzheimers Dement Diagn Assess Dis Monit 10:471. https://doi.org/10.1016/j.dadm.2018.06.002
Sturm VE, Yokoyama JS, Seeley WW et al (2013) Heightened emotional contagion in mild cognitive impairment and Alzheimer’s disease is associated with temporal lobe degeneration. Proc Natl Acad Sci U S A 110:9944–9949. https://doi.org/10.1073/pnas.1301119110
Healey ML, Grossman M (2018) Cognitive and affective perspective-taking: evidence for shared and dissociable anatomical substrates. Front Neurol 9:491
Qureshi AW, Monk RL (2018) Executive function underlies both perspective selection and calculation in level-1 visual perspective taking. Psychon Bull Rev 25:1526–1534. https://doi.org/10.3758/s13423-018-1496-8
Brown-Schmidt S (2009) The role of executive function in perspective taking during online language comprehension. Psychon Bull Rev 16:893–900. https://doi.org/10.3758/PBR.16.5.893
Duclos H, Bejanin A, Eustache F et al (2018) Role of context in affective theory of mind in Alzheimer’s disease. Neuropsychologia 119:363–372. https://doi.org/10.1016/j.neuropsychologia.2018.08.025
Demichelis OP, Coundouris SP, Grainger SA, Henry JD (2020) Empathy and theory of mind in Alzheimer’s disease: a meta-analysis. J Int Neuropsychol Soc 26:963–977. https://doi.org/10.1017/S1355617720000478
Ossenkoppele R, Singleton EH, Groot C et al (2022) Research criteria for the behavioral variant of Alzheimer disease: a systematic review and meta-analysis. JAMA Neurol 79:48–60. https://doi.org/10.1001/jamaneurol.2021.4417
Townley RA, Graff-Radford J, Mantyh WG et al (2020) Progressive dysexecutive syndrome due to Alzheimer’s disease: a description of 55 cases and comparison to other phenotypes. Brain Commun 2:fcaa068. https://doi.org/10.1093/braincomms/fcaa068
Singleton EH (2023) Social cognition deficits and biometric signatures in the behavioural variant of Alzheimer’s disease. Brain 146:2163–2174
Montembeault M, Brando E, Charest K et al (2022) Multimodal emotion perception in young and elderly patients with multiple sclerosis. Mult Scler Relat Disord 58:103478. https://doi.org/10.1016/j.msard.2021.103478
Geraudie A, Pressman PS, Pariente J et al (2023) Expressive prosody in patients with focal anterior temporal neurodegeneration. Neurology 101:e825–e835. https://doi.org/10.1212/WNL.0000000000207516
Harding E, Sullivan MP, Woodbridge R et al (2018) ‘Because my brain isn’t as active as it should be, my eyes don’t always see’: a qualitative exploration of the stress process for those living with posterior cortical atrophy. BMJ Open 8:e018663. https://doi.org/10.1136/bmjopen-2017-018663
Acknowledgements
The NACC database is funded by NIA/NIH Grant U24 AG072122. NACC data are contributed by the NIA-funded ADRCs: P30 AG062429 (PI James Brewer, MD, PhD), P30 AG066468 (PI Oscar Lopez, MD), P30 AG062421 (PI Bradley Hyman, MD, PhD), P30 AG066509 (PI Thomas Grabowski, MD), P30 AG066514 (PI Mary Sano, PhD), P30 AG066530 (PI Helena Chui, MD), P30 AG066507 (PI Marilyn Albert, PhD), P30 AG066444 (PI John Morris, MD), P30 AG066518 (PI Jeffrey Kaye, MD), P30 AG066512 (PI Thomas Wisniewski, MD), P30 AG066462 (PI Scott Small, MD), P30 AG072979 (PI David Wolk, MD), P30 AG072972 (PI Charles DeCarli, MD), P30 AG072976 (PI Andrew Saykin, PsyD), P30 AG072975 (PI David Bennett, MD), P30 AG072978 (PI Neil Kowall, MD), P30 AG072977 (PI Robert Vassar, PhD), P30 AG066519 (PI Frank LaFerla, PhD), P30 AG062677 (PI Ronald Petersen, MD, PhD), P30 AG079280 (PI Eric Reiman, MD), P30 AG062422 (PI Gil Rabinovici, MD), P30 AG066511 (PI Allan Levey, MD, PhD), P30 AG072946 (PI Linda Van Eldik, PhD), P30 AG062715 (PI Sanjay Asthana, MD, FRCP), P30 AG072973 (PI Russell Swerdlow, MD), P30 AG066506 (PI Todd Golde, MD, PhD), P30 AG066508 (PI Stephen Strittmatter, MD, PhD), P30 AG066515 (PI Victor Henderson, MD, MS), P30 AG072947 (PI Suzanne Craft, PhD), P30 AG072931 (PI Henry Paulson, MD, PhD), P30 AG066546 (PI Sudha Seshadri, MD), P20 AG068024 (PI Erik Roberson, MD, PhD), P20 AG068053 (PI Justin Miller, PhD), P20 AG068077 (PI Gary Rosenberg, MD), P20 AG068082 (PI Angela Jefferson, PhD), P30 AG072958 (PI Heather Whitson, MD), P30 AG072959 (PI James Leverenz, MD).
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Conceptualization: M-AS-G and MM; Methodology: M-AS-G and MM; Software: M-AS-G, LW and TC; Formal analysis and investigation: M-AS-G and MM; Writing—original draft preparation: M-AS-G and MM; Writing—review and editing: LW, MC, RM, TC; Supervision: MM.
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St-Georges, MA., Wang, L., Chapleau, M. et al. Social cognition and behavioral changes in patients with posterior cortical atrophy. J Neurol 271, 1439–1450 (2024). https://doi.org/10.1007/s00415-023-12089-z
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DOI: https://doi.org/10.1007/s00415-023-12089-z