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Impaired Recognition of Facial and Vocal Emotions in Mild Cognitive Impairment

Published online by Cambridge University Press:  04 March 2021

Helena S. Moreira ,
Ana Sofia Costa Open the ORCID record for Ana Sofia Costa [Opens in a new window] ,
Álvaro Machado ,
São Luís Castro ,
Selene G. Vicente  and
César F. Lima Open the ORCID record for César F. Lima [Opens in a new window]
Helena S. Moreira
Affiliation:
Center for Psychology at the University of Porto, Faculty of Psychology and Educational Sciences, University of Porto, Rua Alfredo Allen 4200-135, Porto, Portugal
Ana Sofia Costa
Affiliation:
Neurocognition Unit, Department of Neurology, Hospital de Braga, Rua das Comunidades Lusíadas 133, Braga, Portugal Department of Neurology, RWTH Aachen University Hospital, Pauwelsstr. 30, 52074Aachen, Germany JARA BRAIN Institute Molecular Neuroscience and Neuroimaging, Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52425Jülich, Germany
Álvaro Machado
Affiliation:
Neurocognition Unit, Department of Neurology, Hospital de Braga, Rua das Comunidades Lusíadas 133, Braga, Portugal
São Luís Castro
Affiliation:
Center for Psychology at the University of Porto, Faculty of Psychology and Educational Sciences, University of Porto, Rua Alfredo Allen 4200-135, Porto, Portugal
Selene G. Vicente*
Affiliation:
Center for Psychology at the University of Porto, Faculty of Psychology and Educational Sciences, University of Porto, Rua Alfredo Allen 4200-135, Porto, Portugal
César F. Lima*
Affiliation:
Instituto Universitário de Lisboa (ISCTE-IUL), Av. das Forças Armadas, 1649-026Lisboa, Portugal
*
*Correspondence and reprint requests to: C. F. Lima, Instituto Universitário de Lisboa (ISCTE-IUL), Avenida das Forças Armadas, 1649-026Lisboa, Portugal. E-mail: [email protected] or S. Vicente, Faculdade de Psicologia e de Ciências da Educação da Universidade do Porto (FPCE-UP), Rua Alfredo Allen, 4200-135Porto, Portugal. E-mail: [email protected]
*Correspondence and reprint requests to: C. F. Lima, Instituto Universitário de Lisboa (ISCTE-IUL), Avenida das Forças Armadas, 1649-026Lisboa, Portugal. E-mail: [email protected] or S. Vicente, Faculdade de Psicologia e de Ciências da Educação da Universidade do Porto (FPCE-UP), Rua Alfredo Allen, 4200-135Porto, Portugal. E-mail: [email protected]
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Abstract

Objective:

The ability to recognize others’ emotions is a central aspect of socioemotional functioning. Emotion recognition impairments are well documented in Alzheimer’s disease and other dementias, but it is less understood whether they are also present in mild cognitive impairment (MCI). Results on facial emotion recognition are mixed, and crucially, it remains unclear whether the potential impairments are specific to faces or extend across sensory modalities,

Method:

In the current study, 32 MCI patients and 33 cognitively intact controls completed a comprehensive neuropsychological assessment and two forced-choice emotion recognition tasks, including visual and auditory stimuli. The emotion recognition tasks required participants to categorize emotions in facial expressions and in nonverbal vocalizations (e.g., laughter, crying) expressing neutrality, anger, disgust, fear, happiness, pleasure, surprise, or sadness.

Results:

MCI patients performed worse than controls for both facial expressions and vocalizations. The effect was large, similar across tasks and individual emotions, and it was not explained by sensory losses or affective symptomatology. Emotion recognition impairments were more pronounced among patients with lower global cognitive performance, but they did not correlate with the ability to perform activities of daily living.

Conclusions:

These findings indicate that MCI is associated with emotion recognition difficulties and that such difficulties extend beyond vision, plausibly reflecting a failure at supramodal levels of emotional processing. This highlights the importance of considering emotion recognition abilities as part of standard neuropsychological testing in MCI, and as a target of interventions aimed at improving social cognition in these patients.

Keywords

EmotionEmotion recognitionMild cognitive impairmentFaceVoice
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 28 , Issue 1 , January 2022 , pp. 48 - 61
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

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Footnotes

Selene G. Vicente and César F. Lima contributed equally to this work.

References

REFERENCES

Anikin, A. & Lima, C.F. (2018). Perceptual and acoustic differences between authentic and acted nonverbal emotional vocalizations. Quarterly Journal of Experimental Psychology, 71, 622–641. https://doi.org/10.1080/17470218.2016.1270976 Google ScholarPubMed
Army Individual Test Battery (1994). Manual of Directions and Scoring. Washington, DC: War Department, Adjutant General’s Office.Google Scholar
Babins, L., Slater, M-E., Whitehead, V., & Chertkow, H. (2008). Can an 18-point clock-drawing scoring system predict dementia in elderly individuals with mild cognitive impairment? Journal of Clinical and Experimental Neuropsychology, 30, 173–186. https://doi.org/10.1080/13803390701336411 CrossRefGoogle ScholarPubMed
Bediou, B., Ryff, I., Mercier, B., Milliery, M., Hénaff, M.-A., D’Amato, T., … Krolak-Salmon, P. (2009). Impaired social cognition in mild Alzheimer disease. Journal of Geriatric Psychiatry and Neurology, 22, 130–140. https://doi.org/10.1177/0891988709332939 CrossRefGoogle ScholarPubMed
Bora, E. & Yener, G.G. (2017). Meta-analysis of social cognition in mild cognitive impairment. Journal of Geriatric Psychiatry and Neurology, 30, 206–213. https://doi.org/10.1177/0891988717710337 CrossRefGoogle ScholarPubMed
Bora, E., Velakoulis, D., & Walterfang, M. (2016). Meta-analysis of facial emotion recognition in behavioral variant frontotemporal dementia: Comparison with Alzheimer disease and healthy controls. Journal of Geriatric Psychiatry and Neurology, 29, 205–211. https://doi.org/10.1177/0891988716640375 CrossRefGoogle ScholarPubMed
Brück, C., Kreifelts, B., & Wildgruber, D. (2011). Emotional voices in context: A neurobiological model of multimodal affective information processing. Physics of Life Reviews, 8, 383–403. https://doi.org/10.1016/j.plrev.2011.10.002 CrossRefGoogle ScholarPubMed
Bucks, R.S. & Radford, S.A. (2004) Emotion processing in Alzheimer’s disease. Aging & Mental Health, 8, 222–232. https://doi.org/10.1080/13607860410001669750 CrossRefGoogle ScholarPubMed
Carton, J.S., Kessler, E.A., & Pape, C.L. (1999). Nonverbal decoding skills and relationship well-being in adults. Journal of Nonverbal Behavior, 23, 91–100. https://doi.org/10.1023/A:1021339410262 CrossRefGoogle Scholar
Cavaco, S., Goncalves, A., Pinto, C., Almeida, E., Gomes, F., Moreira, I., … Teixeira-Pinto, A. (2013a). Trail making test: Regression-based norms for the Portuguese population. Archives of Clinical Neuropsychology, 28, 189–198. https://doi.org/10.1093/arclin/acs115 CrossRefGoogle ScholarPubMed
Cavaco, S., Gonçalves, A., Pinto, C., Almeida, E., Gomes, F., Moreira, I., … Teixeira-Pinto, A. (2013b). Semantic fluency and phonemic fluency: Regression-based norms for the Portuguese population. Archives of Clinical Neuropsychology, 28, 262–271. http://doi.org/10.1093/arclin/act001 CrossRefGoogle ScholarPubMed
Cotter, J., Granger, K., Backx, R., Hobbs, M., Looi, C.Y., & Barnett, J.H. (2018). Social cognitive dysfunction as a clinical marker: A systematic review of meta-analyses across 30 clinical conditions. Neuroscience & Biobehavioral Reviews, 84, 92–99. https://doi.org/10.1016/j.neubiorev.2017.11.014 CrossRefGoogle ScholarPubMed
Dalili, M.N., Penton-Voak, I.S., Harmer, C.J., & Munafò, M.R. (2015). Meta-analysis of emotion recognition deficits in major depressive disorder. Psychological Medicine, 45, 1135–1144. https://doi.org/10.1017/S0033291714002591 CrossRefGoogle ScholarPubMed
Dodich, A., Cerami, C., Crespi, C., Canessa, N., Lettieri, G., Iannaccone, S., … Cacioppo, J.T. (2016). Differential impairment of cognitive and affective mentalizing abilities in neurodegenerative dementias: Evidence from behavioral variant of frontotemporal dementia, Alzheimer’s disease, and mild cognitive impairment. Journal of Alzheimer’s Disease, 50, 1011–1022. https://doi.org/10.3233/jad-150605 CrossRefGoogle ScholarPubMed
Drapeau, J., Gosselin, N., Gagnon, L., Peretz, I., & Lorrain, D. (2009). Emotional recognition from face, voice, and music in dementia of the Alzheimer type. Annals of the New York Academy of Sciences, 1169, 342–345. https://doi.org/10.1111/j.1749-6632.2009.04768.x CrossRefGoogle ScholarPubMed
Duara, R., Loewenstein, D.A., Potter, E., Appel, J., Greig, M.T., Urs, R., … Potter, H. (2008). Medial temporal lobe atrophy on MRI scans and the diagnosis of Alzheimer disease. Neurology, 71, 1986–1992. https://doi.org/10.1212/01.wnl.0000336925.79704.9f CrossRefGoogle Scholar
Edmonds, E.C., Eppig, J., Bondi, M.W., Leyden, K.M., Goodwin, B., Delano-Wood, L., … Alzheimer’s Disease Neuroimaging Initiative (2016). Heterogeneous cortical atrophy patterns in MCI not captured by conventional diagnostic criteria. Neurology, 87, 2108–2116. https://doi.org/10.1212/WNL.0000000000003326 CrossRefGoogle Scholar
Eisenbarth, H. & Alpers, G.W. (2011). Happy mouth and sad eyes: Scanning emotional facial expressions. Emotion, 11, 860–865. https://doi.org/10.1037/a0022758 CrossRefGoogle ScholarPubMed
Faul, F., Erdfelder, E., Buchner, A., & Lang, A.-G. (2009). Statistical power analyses using G*Power 3.1: Tests for correlation and regression analyses. Behavior Research Methods, 41, 1149–1160. https://doi.org/10.3758/brm.41.4.1149 CrossRefGoogle ScholarPubMed
Fernandes, S. (2013). Teste de Cores e Palavras de Stroop. Lisboa: Cegoc-TEA.Google Scholar
Fide, E., Emek-Savaş, D.D., Aktürk, T., Güntekin, B., Hanoğlu, L., & Yener, G.G. (2019). Electrophysiological evidence of altered facial expressions recognition in Alzheimer’s disease: A comprehensive ERP study. Clinical Neurophysiology, 130, 1813–1824. https://doi.org/10.1016/j.clinph.2019.06.229 CrossRefGoogle ScholarPubMed
Filipe, M.G., Frota, S., Villagomez, A., & Vicente, S.G. (2016). Prosody in Portuguese children with high-functioning autism. In Armstrong, M., Henriksen, N.C., & Vanrell, M.M. (Eds.), Intonational Grammar in Ibero-Romance: Approaches Across Linguistic Subfields (pp. 277–294). Philadelphia, USA: John Benjamins. doi: 10.1075/ihll.6.13fil.Google Scholar
Fittipaldi, S., Ibanez, A., Baez, S., Manes, F., Sedeno, L., & García, A.M. (2019). More than words: Social cognition across variants of primary progressive aphasia. Neuroscience & Biobehavioral Reviews, 100, 263–284. https://doi.org/10.1016/j.neubiorev.2019.02.020 CrossRefGoogle ScholarPubMed
Folstein, M.F., Folstein, S.E., and 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. https://doi.org/10.1016/0022-3956(75)90026-6 CrossRefGoogle ScholarPubMed
Freitas, S, Simões, M.R., Alves, L, & Santana, I. (2013). Montreal Cognitive Assessment: Validation study for mild cognitive impairment and Alzheimer disease. Alzheimer Disease and Associated Disorders, 27, 37–43. https://doi.org/10.1097/wad.0b013e3182420bfe CrossRefGoogle ScholarPubMed
Freitas, S., Simões, M.R., Alves, L., & Santana, I. (2015). The relevance of sociodemographic and health variables on MMSE normative data. Applied Neuropsychology: Adult, 22, 311–319. https://doi.org/10.1080/23279095.2014.926455 CrossRefGoogle ScholarPubMed
Frühholz, S., Trost, W., & Kotz, S.A. (2016). The sound of emotions - Towards a unifying neural network perspective of affective sound processing. Neuroscience & Biobehavioral Reviews, 68, 96–110. https://doi.org/10.1016/j.neubiorev.2016.05.002 CrossRefGoogle ScholarPubMed
Gallagher, D., Fischer, C.E., & Iaboni, A. (2017). Neuropsychiatric symptoms in mild cognitive impairment. Canadian Journal of Psychiatry, 62, 161–169. https://doi.org/10.1177/0706743716648296 CrossRefGoogle ScholarPubMed
Gauthier, S., Reisberg, B., Zaudig, M., Petersen, R.C., Ritchie, K., Broich, K., … Cummings, J.L. (2006). Mild cognitive impairment. The Lancet, 367, 1262–1270. https://doi.org/10.1016/S0140-6736(06)68542-5 CrossRefGoogle ScholarPubMed
Geda, Y.E., Roberts, R.O., Knopman, D.S., Petersen, R.C., Christianson, T.J., Pankratz, V.S., … Rocca, W.A. (2008). Prevalence of neuropsychiatric symptoms in mild cognitive impairment and normal cognitive aging: Population-based study. Archives of General Psychiatry, 65, 1193–1198. https://doi.org/10.1001/archpsyc.65.10.1193 CrossRefGoogle ScholarPubMed
Ghosh, B.C., Rowe, J.B., Calder, A.J., Hodges, J.R., & Bak, T.H. (2009). Emotion recognition in progressive supranuclear palsy. Journal of Neurology, Neurosurgery, and Psychiatry, 80, 1143–1145. https://doi.org/10.1136/jnnp.2008.155846 CrossRefGoogle ScholarPubMed
Goeleven, E., De Raedt, R., Leyman, L., & Verschuere, B. (2008). The Karolinska directed emotional faces: A validation study. Cognition and Emotion, 22, 1094–1118. https://doi.org/10.1080/02699930701626582 CrossRefGoogle Scholar
Golden, C.J., & Freshwater, S.M. (1978). The Stroop Color and Word Test: A Manual for Clinical and Experimental Uses. Chicago, IL: Stoelting Google Scholar
Goodkind, M.S., Sturm, V.E., Ascher, E.A., Shdo, S.M., Miller, B.L., Rankin, K.P., & Levenson, R.W. (2015). Emotion recognition in frontotemporal dementia and Alzheimer’s disease: A new film-based assessment. Emotion, 15, 416–427. https://doi.org/10.1037/a0039261 CrossRefGoogle ScholarPubMed
Gray, H.M., & Tickle-Degnen, L. (2010). A meta-analysis of performance on emotion recognition tasks in Parkinson’s disease. Neuropsychology, 24, 176–191. https://doi.org/10.1037/a0018104 CrossRefGoogle ScholarPubMed
Halberstadt, J., Ruffman, T., Murray, J., Taumoepeau, M., & Ryan, M. (2011). Emotion perception explains age-related differences in the perception of social gaffes. Psychology and Aging, 26, 133–136. https://doi.org/10.1037/a0021366 CrossRefGoogle ScholarPubMed
Hall, J.A., Andrzejewski, S.A., & Yopchick, J.E. (2009). Psychosocial correlates of interpersonal sensitivity: A meta-analysis. Journal of Nonverbal Behavior, 33, 149–180. https://doi.org/10.1007/s10919-009-0070-5 CrossRefGoogle Scholar
Hallam, B.J., Silverberg, N.D., LaMarre, A.K., Mackenzie, I.R. A., & Feldman, H.H. (2008). Clinical presentation of prodromal frontotemporal dementia. American Journal of Alzheimer’s Disease & Other Dementias, 22, 456–467. https://doi.org/10.1177/1533317507308781 CrossRefGoogle Scholar
Hämäläinen, A., Tervo, S., Grau-Olivares, M., Niskanen, E., Pennanen, C., Huuskonen, J., … Soininen, H. (2007). Voxel-based morphometry to detect brain atrophy in progressive mild cognitive impairment. NeuroImage, 37, 1122–1131. https://doi.org/10.1016/j.neuroimage.2007.06.016 CrossRefGoogle ScholarPubMed
Henry, J.D., Thompson, C., Rendell, P.G., Phillips, L.H., Carbert, J., Sachdev, P., & Brodaty, H. (2012). Perception of biological motion and emotion in mild cognitive impairment and dementia. Journal of the International Neuropsychological Society, 18, 866–873. https://doi.org/10.1017/S1355617712000665 CrossRefGoogle ScholarPubMed
Hessen, E., Reinvang, I., Eliassen, C.F., Nordlund, A., Gjerstad, L., Fladby, T., & Wallin, A. (2014). The combination of dysexecutive and amnestic deficits strongly predicts conversion to dementia in young mild cognitive impairment patients: A report from the Gothenburg-Oslo MCI study. Dementia and Geriatric Cognitive Disorders, 4, 76–85. https://doi.org/10.1159/000360282 CrossRefGoogle ScholarPubMed
Hoekert, M., Kahn, R.S., Pijnenborg, M., & Aleman, A. (2007). Impaired recognition and expression of emotional prosody in schizophrenia: Review and meta-analysis. Schizophrenia Research, 96, 135–145. https://doi.org/10.1016/j.schres.2007.07.023 CrossRefGoogle ScholarPubMed
Isaacowitz, D.M., Löckenhoff, C.E., Lane, R.D., Wright, R., Sechrest, L., Riedel, R., & Costa, P.T. (2007). Age differences in recognition of emotion in lexical stimuli and facial expressions. Psychology and Aging, 22, 147–159. https://doi.org/10.1037/0882-7974.22.1.147 CrossRefGoogle ScholarPubMed
Ismail, Z., Elbayoumi, H., Fischer, C.E., Hogan, D.B., Millikin, C.P., Schweizer, T., … Fiest, K.M. (2017). Prevalence of depression in patients with mild cognitive impairment. JAMA Psychiatry, 74, 58. https://doi.org/10.1001/jamapsychiatry.2016.3162 CrossRefGoogle ScholarPubMed
Jarosz, A.F., & Wiley, J. (2014). What are the odds? A practical guide to computing and reporting bayes factors. The Journal of Problem Solving, 7, 2–9. https://doi.org/10.7771/1932-6246.1167 CrossRefGoogle Scholar
JASP Team (2019). JASP (Version 0.11.1) [Computer software].Google Scholar
Klein-Koerkamp, Y., Beaudoin, M., Baciu, M., & Hot, P. (2012). Emotional decoding abilities in Alzheimer’s disease: A meta-analysis. Journal of Alzheimer’s Disease, 32, 109–125. https://doi.org/10.3233/jad-2012-120553 CrossRefGoogle ScholarPubMed
Lee, G., Nho, K., Kang, B., Sohn, K.-A., & Kim, D. (2019). Predicting Alzheimer’s disease progression using multi-modal deep learning approach. Scientific Reports, 9, 1952. https://doi.org/10.1038/s41598-018-37769-z CrossRefGoogle ScholarPubMed
Lima, C.F., Alves, T., Scott, S.K., & Castro, S.L. (2014). In the ear of the beholder: How age shapes emotion processing in nonverbal vocalizations. Emotion, 14, 145–160. https://doi.org/10.1037/a0034287 CrossRefGoogle ScholarPubMed
Lima, C.F., Anikin, A., Monteiro, A.C., Scott, S.K., & Castro, S.L. (2019). Automaticity in the recognition of nonverbal emotional vocalizations. Emotion, 19, 219–233. https://doi.org/10.1037/emo0000429 CrossRefGoogle ScholarPubMed
Lima, C.F., Brancatisano, O., Fancourt, A., Müllensiefen, D., Scott, S.K., Warren, J.D., & Stewart, L. (2016). Impaired socio-emotional processing in a developmental music disorder. Scientific Reports, 6, 34911.https://doi.org/10.1038/srep34911 CrossRefGoogle Scholar
Lima, C.F., Castro, S.L., & Scott, S.K. (2013). When voices get emotional: A corpus of nonverbal vocalizations for research on emotion processing. Behavior Research Methods, 45, 1234–1245. https://doi.org/10.3758/s13428-013-0324-3 CrossRefGoogle ScholarPubMed
Lima, C.F., Garret, C., & Castro, S.L. (2013). Not all sounds sound the same: Parkinson’s disease affects differently emotion processing in music and in speech prosody. Journal of Clinical and Experimental Neuropsychology, 35, 373–392. https://doi.org/10.1080/13803395.2013.776518 CrossRefGoogle ScholarPubMed
Lin, F.R., Niparko, J.K., & Ferrucci, L. (2011). Hearing loss prevalence in the United States. Archives of Internal Medicine, 171, 1851–1852. https://doi.org/10.1001/archinternmed.2011.506 CrossRefGoogle ScholarPubMed
Markesbery, W.R. (2010). Neuropathologic alterations in mild cognitive impairment: A review. Journal of Alzheimer’s Disease, 19, 221–228. https://doi.org/10.3233/JAD-2010-1220 CrossRefGoogle ScholarPubMed
McCade, D., Savage, G., & Naismith, S.L. (2011). Review of emotion recognition in mild cognitive impairment. Dementia and Geriatric Cognitive Disorders, 32, 257–266. https://doi.org/10.1159/000335009 CrossRefGoogle ScholarPubMed
McCade, D., Savage, G., Guastella, A., Lewis, S.J. G., & Naismith, S.L. (2013). Emotion recognition deficits exist in mild cognitive impairment, but only in the amnestic subtype. Psychology and Aging, 28, 840–852. https://doi.org/10.1037/a0033077 CrossRefGoogle ScholarPubMed
McLellan, T., Johnston, L., Dalrymple-Alford, J., & Porter, R. (2008). The recognition of facial expressions of emotion in Alzheimer’s disease: A review of findings. Acta Neuropsychiatrica, 20, 236–250. https://doi.org/10.1111/j.1601-5215.2008.00315.x CrossRefGoogle ScholarPubMed
Michaud, T.L., Su, D., Siahpush, M., & Murman, D.L. (2017). The risk of incident mild cognitive impairment and progression to dementia considering mild cognitive impairment subtypes. Dementia and Geriatric Cognitive Disorders, 7, 15–29. https://doi.org/10.1159/000452486 CrossRefGoogle ScholarPubMed
Monastero, R., Cicero, C.E., Baschi, R., Davì, M., Luca, A., Restivo, V., … Nicoletti, A. (2018). Mild cognitive impairment in Parkinson’s disease: The Parkinson’s disease cognitive study (PACOS). Journal of Neurology, 265, 1050–1058. https://doi.org/10.1007/s00415-018-8800-4 CrossRefGoogle Scholar
Monastero, R., Mangialasche, F., Camarda, C., Ercolani, S., & Camarda, R. (2009). A systematic review of neuropsychiatric symptoms in mild cognitive impairment. Journal of Alzheimer’s Disease, 18, 11–30. https://doi.org/10.3233/jad-2009-1120 CrossRefGoogle ScholarPubMed
Moradi, Z., Najlerahim, A., & Humphreys, G. (2018). Preserved recognition and selection of facial expression of happiness in mild Alzheimer’s Disease. Alzheimer’s, Dementia & Cognitive Neurology, 2, 1–8. https://doi.org/10.15761/adcn.1000119 Google Scholar
Moreira, H.S., Lima, C.F., & Vicente, S.G. (2014). Examining Executive Dysfunction with the Institute of Cognitive Neurology (INECO) Frontal Screening (IFS): Normative values from a healthy sample and clinical utility in Alzheimer’s Disease. Journal of Alzheimer’s Disease, 42, 261–273. https://doi.org/10.3233/jad-132348 CrossRefGoogle ScholarPubMed
Nag, S., Yu, L., Capuano, A.W., Wilson, R.S., Leurgans, S.E., Bennett, D.A., & Schneider, J.A. (2015). Hippocampal sclerosis and TDP-43 pathology in aging and Alzheimer disease. Annals of Neurology, 77, 942–952. https://doi.org/10.1002/ana.24388 CrossRefGoogle ScholarPubMed
Nasreddine, Z.S., Phillips, N.A., Bédirian, V., Charbonneau, S., Whitehead, V., Collin, I., … Chertkow, H. (2005). The Montreal Cognitive Assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53, 695–699. https://doi.org/10.1111/j.1532-5415.2005.53221.x CrossRefGoogle ScholarPubMed
Nordlund, A., Rolstad, S., Klang, O., Edman, A., Hansen, S., & Wallin, A. (2009). Two-year outcome of MCI subtypes and aetiologies in the Goteborg MCI study. Journal of Neurology, Neurosurgery & Psychiatry, 81, 541–546. https://doi.org/10.1136/jnnp.2008.171066 CrossRefGoogle ScholarPubMed
Pais-Ribeiro, J., Silva, I., Ferreira, T., Martins, A., Meneses, R., & Baltar, M. (2007). Validation study of a Portuguese version of the Hospital Anxiety and Depression Scale. Psychology, Health & Medicine, 12, 225–237. https://doi.org/10.1080/13548500500524088 CrossRefGoogle ScholarPubMed
Palmer, K., Bäckman, L., Winblad, B., & Fratiglioni, L. (2008). Mild cognitive impairment in the general population: Occurrence and progression to Alzheimer disease. The American Journal of Geriatric Psychiatry, 16, 603–611. https://doi.org/10.1016/j.jalz.2008.05.790 CrossRefGoogle ScholarPubMed
Park, S., Kim, T., Shin, S.A., Kim, Y.K., Sohn, B.K., Park, H.J., Youn, J.H., & Lee, J.Y. (2017). Behavioral and neuroimaging evidence for facial emotion recognition in elderly Korean adults with mild cognitive impairment, Alzheimer’s disease, and frontotemporal dementia. Frontiers in Aging Neuroscience, 9, 389. https://doi.org/10.3389/fnagi.2017.00389 CrossRefGoogle ScholarPubMed
Peelen, M.V., Atkinson, A.P., & Vuilleumier, P. (2010). Supramodal representations of perceived emotions in the human brain. The Journal of Neuroscience, 30, 10127–10134. https://doi.org/10.1523/JNEUROSCI.2161-10.2010 CrossRefGoogle ScholarPubMed
Petersen, R.C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183–194. https://doi.org/10.1111/j.1365-2796.2004.01388.x CrossRefGoogle ScholarPubMed
Petersen, R.C., Caracciolo, B., Brayne, C., Gauthier, S., Jelic, V., & Fratiglioni, L. (2014). Mild cognitive impairment: A concept in evolution. Journal of Internal Medicine, 275, 214–228. https://doi.org/10.1111/joim.12190 CrossRefGoogle Scholar
Petersen, R.C., Roberts, R.O., Knopman, D.S., Boeve, B.F., Geda, Y.E., Ivnik, R.J., Smith, G.E., & Jack, C.R. (2009). Mild cognitive impairment: Ten years later. Archives of Neurology, 66, 1447–1455. https://doi.org/10.1001/archneurol.2009.266 CrossRefGoogle ScholarPubMed
Petersen, R.C., Smith, G.E., Waring, S.C., Ivnik, R.J., Tangalos, E.G., & Kokmen, E. (1999). Mild cognitive impairment. Archives of Neurology, 56, 303. https://doi.org/10.1001/archneur.56.3.303 CrossRefGoogle ScholarPubMed
Phillips, L.H., Scott, C., Henry, J.D., Mowat, D., & Bell, J.S. (2010). Emotion perception in Alzheimer’s disease and mood disorder in old age. Psychology and Aging, 25, 38–47. https://doi.org/10.1037/a0017369 CrossRefGoogle ScholarPubMed
Pietschnig, J., Aigner-Wöber, R., Reischenböck, N., Kryspin-Exner, I., Moser, D., Klug, S., … Lehrner, J. (2015). Facial emotion recognition in patients with subjective cognitive decline and mild cognitive impairment. International Psychogeriatrics, 28, 477–485. https://doi.org/10.1017/s1041610215001520 CrossRefGoogle ScholarPubMed
Richard-Mornas, A., Borg, C., Klein-Koerkamp, Y., Paignon, A., Hot, P., & Thomas-Antérion, C. (2012). Perceived eye region and the processing of fearful expressions in mild cognitive impairment patients. Dementia and Geriatric Cognitive Disorders, 33, 43–49. https://doi.org/10.1159/000336599 CrossRefGoogle ScholarPubMed
Roberts, R.O., Knopman, D.S., Mielke, M.M., Cha, R.H., Pankratz, V.S., Christianson, T.J., Geda, Y.E., Boeve, B.F., Ivnik, R.J., Tangalos, E.G., Rocca, W.A., & Petersen, R.C. (2014). Higher risk of progression to dementia in mild cognitive impairment cases who revert to normal. Neurology, 82, 317–325. https://doi.org/10.1212/WNL.0000000000000055 CrossRefGoogle ScholarPubMed
Rozzini, L., Chilovi, B.V., Peli, M., Conti, M., Rozzini, R., Trabucchi, M., & Padovani, A. (2009). Anxiety symptoms in mild cognitive impairment. International Journal of Geriatric Psychiatry, 24, 300–305.https://doi.org/10.1002/gps.2106 CrossRefGoogle ScholarPubMed
Ruffman, T., Henry, J.D., Livingstone, V., & Phillips, L.H. (2008). A meta-analytic review of emotion recognition and aging: Implications for neuropsychological models of aging. Neuroscience & Biobehavioral Reviews, 32, 863–881. https://doi.org/10.1016/j.neubiorev.2008.01.001 CrossRefGoogle ScholarPubMed
Ruffman, T., Murray, J., Halberstadt, J., & Taumoepeau, M. (2010). Verbosity and emotion recognition in older adults. Psychology and Aging, 25, 492–497. https://doi.org/10.1037/a0018247 CrossRefGoogle ScholarPubMed
Santana, I., Duro, D., Freitas, S., Alves, L., & Simões, M.R. (2013). The Clock Drawing Test: Portuguese norms, by age and education, for three different scoring systems. Archives of Clinical Neuropsychology, 28, 375–387. https://doi.org/10.1093/arclin/act016 CrossRefGoogle ScholarPubMed
Sarabia-Cobo, C.M., García-Rodríguez, B., Navas, M.J., & Ellgring, H. (2015). Emotional processing in patients with mild cognitive impairment: The influence of the valence and intensity of emotional stimuli. Journal of the Neurological Sciences, 357, 222–228. https://doi.org/10.1016/j.jns.2015.07.034 CrossRefGoogle ScholarPubMed
Sauter, D.A., Eisner, F., Ekman, P., & Scott, S.K. (2010). Cross-cultural recognition of basic emotions through nonverbal emotional vocalizations. Proceedings of the National Academy of Sciences of the United States of America, 107, 2408–2412. https://doi.org/10.1073/pnas.0908239106 CrossRefGoogle ScholarPubMed
Savage, S., Hsieh, S., Leslie, F., Foxe, D., Piguet, O., & Hodges, J.R. (2013). Distinguishing subtypes in primary progressive aphasia: Application of the Sydney Language Battery. Dementia and Geriatric Cognitive Disorders, 35, 208–218. https://doi.org/10.1159/000346389 CrossRefGoogle ScholarPubMed
Scherer, K.R. (1995). Expression of emotion in voice and music. Journal of Voice, 9, 235–248. https://doi.org/10.1016/s0892-1997(05)80231-0 CrossRefGoogle ScholarPubMed
Schirmer, A. (2018). Is the voice an auditory face? An ALE meta-analysis comparing vocal and facial emotion processing. Social Cognitive and Affective Neuroscience, 13, 1–13. https://doi.org/10.1093/scan/nsx142 CrossRefGoogle ScholarPubMed
Schirmer, A. & Adolphs, R. (2017). Emotion perception from face, voice, and touch: Comparisons and convergence. Trends in Cognitive Sciences, 21, 216–228. https://doi.org/10.1016/j.tics.2017.01.001 CrossRefGoogle ScholarPubMed
Schirmer, A., & Kotz, S.A. (2006). Beyond the right hemisphere: Brain mechanisms mediating vocal emotional processing. Trends in Cognitive Sciences, 10, 24–30. https://doi.org/10.1016/j.tics.2005.11.009 CrossRefGoogle ScholarPubMed
Scott, S.K., Sauter, D., & McGettigan, C. (2010). Brain mechanisms for processing perceived emotional vocalizations in humans. Handbook of Mammalian Vocalization - An Integrative Neuroscience Approach, 187–197. https://doi.org/10.1016/b978-0-12-374593-4.00019-x CrossRefGoogle Scholar
Shimokawa, A., Yatomi, N., Anamizu, S., Torii, S., Isono, H., Sugai, Y., & Kohno, M. (2001). Influence of deteriorating ability of emotional comprehension on interpersonal behavior in Alzheimer-type dementia. Brain and Cognition, 47, 423–433. https://doi.org/10.1006/brcg.2001.1318 CrossRefGoogle ScholarPubMed
Snaith, R.P. (2003). The hospital anxiety and depression scale. Health and Quality of Life Outcomes, 1, 29. https://doi.org/10.1186/1477-7525-1-29 CrossRefGoogle ScholarPubMed
Snaith, R.P., & Zigmond, A.P. (1994). The Hospital Anxiety and Depression Scale Manual. Windsor: NFER-Nelson. https://doi.org/10.1037/t03589-000 Google Scholar
Sousa, L.B., Simões, M.R., Pires, L., Vilar, M., & Freitas, S. (2008). Inventário de Avaliação Funcional de Adultos e Idosos (IAFAI): Manual de administração e cotacão [Adults and Older Adults Functional Assessment Inventory (IAFAI): Administration and scoring manual]. Coimbra, Portugal: Faculty of Psychology and Educational Sciences—University of Coimbra.Google Scholar
Spoletini, I., Marra, C., DiIulio, F., Gianni, W., Sancesario, G., Giubilei, F., … Spalletta, G. (2008). Facial emotion recognition deficit in amnestic mild cognitive impairment and Alzheimer disease. The American Journal of Geriatric Psychiatry, 16, 389–398. https://doi.org/10.1097/jgp.0b013e318165dbce CrossRefGoogle ScholarPubMed
Steffens, D.C. (2012). Depressive symptoms and mild cognitive impairment in the elderly: An ominous combination. Biological Psychiatry, 71, 762–764. https://doi.org/10.1016/j.biopsych.2012.02.002 CrossRefGoogle Scholar
Stephan, B.C. M., Hunter, S., Harris, D., Llewellyn, D.J., Siervo, M., Matthews, F.E., & Brayne, C. (2012). The neuropathological profile of mild cognitive impairment (MCI): a systematic review. Molecular Psychiatry, 17, 1056–1076. https://doi.org/10.1038/mp.2011.147 CrossRefGoogle ScholarPubMed
Stewart, M.E., McAdam, C., Ota, M., Peppé, S., & Cleland, J. (2013). Emotional recognition in autism spectrum conditions from voices and faces. Autism, 17, 6–14. https://doi.org/10.1177/1362361311424572 CrossRefGoogle ScholarPubMed
Strachan, J.W.A., Sebanz, N., & Knoblich, G. (2019). The role of emotion in the dyad inversion effect. PLoS ONE, 14, e0219185. https://doi.org/10.1371/journal.pone.0219185 CrossRefGoogle ScholarPubMed
Sturm, V.E., Yokoyama, J.S., Seeley, W.W., Kramer, J.H., Miller, B.L., & Rankin, K.P. (2013). Heightened emotional contagion in mild cognitive impairment and Alzheimer’s disease is associated with temporal lobe degeneration. Proceedings of the National Academy of Sciences of the United States of America, 110, 9944–9949. https://doi.org/10.1073/pnas.1301119110 CrossRefGoogle ScholarPubMed
Tabatabaei-Jafari, H., Shaw, M.E., & Cherbuin, N. (2015). Cerebral atrophy in mild cognitive impairment: A systematic review with meta-analysis. Alzheimer’s & Dementia, 1, 487–504. https://doi.org/10.1016/j.dadm.2015.11.002 Google ScholarPubMed
Teng, E., Lu, P.H., & Cummings, J.L. (2007). Deficits in facial emotion processing in mild cognitive impairment. Dementia and Geriatric Cognitive Disorders, 23, 271–279. https://doi.org/10.1159/000100829 CrossRefGoogle ScholarPubMed
Torralva, T., Roca, M., Gleichgerrcht, E., López, P., & Manes, F. (2009). INECO Frontal Screening (IFS): A brief, sensitive, and specific tool to assess executive functions in dementia. Journal of the International Neuropsychological Society, 15, 777–786. https://doi.org/10.1017/s1355617710000883 CrossRefGoogle ScholarPubMed
Uljarevic, M. & Hamilton, A. (2013). Recognition of emotions in autism: a formal meta-analysis. Journal of Autism and Developmental Disorders, 43, 1517–1526. https://doi.org/10.1007/s10803-012-1695-5 CrossRefGoogle ScholarPubMed
Valiengo, L., Stella, F., & Forlenza, O.V. (2016). Mood disorders in the elderly: Prevalence, functional impact, and management challenges. Neuropsychiatric Disease and Treatment, 12, 2105–2114. https://doi.org/10.2147/NDT.S94643 Google Scholar
Virtanen, M., Singh-Manoux, A., Batty, G.D., Ebmeier, K.P., Jokela, M., Harmer, C.J., & Kivimäki, M. (2017). The level of cognitive function and recognition of emotions in older adults. PloS ONE, 12, e0185513. https://doi.org/10.1371/journal.pone.0185513 CrossRefGoogle ScholarPubMed
Wagner, H.L. (1993). On measuring performance in category judgment studies of nonverbal behavior. Journal of Nonverbal Behavior, 17, 3–28. https://doi.org/10.1007/bf00987006 CrossRefGoogle Scholar
Wang, J., Wu, X., Lai, W., Long, E., Zhang, X., Li, W., … Lin, H. (2017). Prevalence of depression and depressive symptoms among outpatients: A systematic review and meta-analysis. BMJ Open, 7, e017173. https://doi.org/10.1136/bmjopen-2017-017173 CrossRefGoogle ScholarPubMed
Ward, A., Tardiff, S., Dye, C., & Arrighi, H.M. (2013). Rate of conversion from prodromal Alzheimer’s disease to Alzheimer’s dementia: A systematic review of the literature. Dementia and Geriatric Cognitive Disorders, 3, 320–332. https://doi.org/10.1159/000354370 CrossRefGoogle ScholarPubMed
Warrington, E.K, & James, M. (1991). The Visual Object and Space Perception Battery. Bury St Edmunds, England: Thames Valley Test Company.Google Scholar
Wechsler, D. (1997). Wechsler Memory Scale - Third Edition. San Antonio, TX: The Psychological Corporation. https://doi.org/10.1037/t27207-000 Google Scholar
Wechsler, D. (2008). WMS–III: Escala de Memória de Wechsler – 3a Edição: Manual técnico. [WMS–III: Wechsler Memory Scale–3rd edition: Technical manual]. Lisboa: Cegoc.Google Scholar
Weiss, E.M., Kohler, C.G., Vonbank, J., Stadelmann, E., Kemmler, G., Hinterhuber, H., & Marksteiner, J. (2008). Impairment in emotion recognition abilities in patients with mild cognitive impairment, early and moderate Alzheimer disease compared with healthy comparison subjects. The American Journal of Geriatric Psychiatry, 16, 974–980. https://doi.org/10.1097/jgp.0b013e318186bd53 CrossRefGoogle ScholarPubMed
Whitwell, J.L., Petersen, R.C., Negash, S., Weigand, S.D., Kantarci, K., Ivnik, R.J., … Jack, C.R. (2007). Patterns of atrophy differ among specific subtypes of mild cognitive impairment. Archives of Neurology, 64, 1130. https://doi.org/10.1001/archneur.64.8.1130 CrossRefGoogle ScholarPubMed
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. https://doi.org/10.1111/j.1365-2796.2004.01380.x CrossRefGoogle Scholar
Young, A.W., Frühholz, S., & Schweinberger, S.R. (2020). Face and voice perception: Understanding commonalities and differences. Trends in Cognitive Sciences, 24, 398–410. https://doi.org/10.1016/j.tics.2020.02.001 CrossRefGoogle ScholarPubMed
Zhang, H., Sachdev, P.S., Wen, W., Kochan, N.A., Crawford, J.D., Brodaty, H., … Trollor, J.N. (2012). Gray matter atrophy patterns of mild cognitive impairment subtypes. Journal of the Neurological Sciences, 315, 26–32. https://doi.org/10.1016/j.jns.2011.12.011 CrossRefGoogle ScholarPubMed