Déficits no processamento emocional na doença de Alzheimer: uma revisão sistemática

Silva, Rogeria Cristina Rangel da; Carvalho, Raquel Luíza Santos de; Dourado, Marcia Cristina Nascimento

doi:10.1590/1980-57642021dn15-030003

Original Article • Dement. neuropsychol. 15 (03) • Jul-Sep 2021 • https://doi.org/10.1590/1980-57642021dn15-030003 linkcopiar

Déficits no processamento emocional na doença de Alzheimer: uma revisão sistemática

Autoria SCIMAGO INSTITUTIONS RANKINGS

O processamento emocional é a habilidade de indivíduos inferirem informação emocional. Não há consenso sobre como a doença de Alzheimer (DA) afeta o processamento emocional.

Objetivo: Este artigo visa revisar sistematicamente o impacto da DA no processamento emocional.

Métodos: Realizamos uma pesquisa com base no Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA). A pesquisa bibliográfica foi realizada nas bases de dados eletrônicas MEDLINE (Pubmed) e Science Citation Index (ISI). Os seguintes descritores foram utilizados no processo de revisão: processamento emocional ou emoção, cognição ou funções cognitivas e doença de Alzheimer. A revisão sistemática foi registrada no Registro Prospectivo Internacional de Revisões Sistemáticas (PROSPERO), sob o número CRD42018115891.

Resultados: Foram identificados 425 artigos, 19 dos quais atendiam aos critérios de inclusão. Os estímulos visuais emocionais foram os mais utilizados entre os estudos. A maioria dos estudos usou tarefas de nomeação emocional, discriminação, identificação e correspondência. Os resultados foram contraditórios. Muitos estudos relataram que indivíduos com DA apresentavam comprometimento em tarefas de percepção emocional, outros resultados apontam para habilidades preservadas. A relação entre o processamento emocional e a cognição também não está clara. Alguns estudos sugerem que o desempenho cognitivo geral afeta o desempenho nas tarefas de percepção emocional na DA, outros estudos demonstraram déficits no reconhecimento da emoção, independentemente do desempenho cognitivo.

Conclusões: Os estudos são escassos, apresentam resultados contraditórios e relatam comprometimento no processamento emocional em relação à cognição. Além disso, análises de correlação entre processamento emocional e funcionamento cognitivo não conseguiram revelar relações claras.

Palavra-chave:
doença de Alzheimer; cognição; emoção

Authors, year	Design	Sample	AD diagnosis	Objective	Emotional processing evaluation	Cognitive evaluation	Quality assessment
Bourgin, 2018⁴¹	Cross-sectional	AD 16 HOAs 25	NINCDS-ADRDA Imaging exams	To determine whether early emotional attention mechanisms are affected by AD.	An eye-tracking technique during a simple but time-constrained cognitive task.	MMSE BDI	*****
Daley, 2018³⁹	Cross-sectional	AD=28 OCs 30	NINCDS-ADRDA	To investigate the relationship between emotional perception abilities in AD participants and CG well-being.	Advanced Clinical Solutions Social Perception subtest (ACS-SP)	Montreal Cognitive Assessment (MoCA).	*****
Dourado, 2019⁵⁶	Cross-sectional	52 participants AD (mild n=29; moderate n=23)	DSM-IV-TR Imaging exams	To compare facial expression recognition in this AD sample and to identify which factors were associated with the impairment of the ability according to disease severity	The protocol FACES	Assessment Scale– Cognitive Subscale (ADAS-Cog), MMSE, Wechsler Digit Span Test, TMT And Semantic fluency tests	*****
Duclos, 2018⁴²	Cross-sectional	n=60 AD 20 HOS 20 and HYS 20	NINCDS-ADRDA	To assess both decoding and reasoning processes in AD, as well as the effect of context on emotion attribution	Peter and Mary emotion tasks Battery	MMSE	*****
Giffard, 2009⁴³	Cross-sectional	AD 26 CG 26	NINCDS-ADRDA	To introduce and control the emotional nature of concepts in order to conduct a more ecological investigation of semantic memory in AD using a semantic and affective priming paradigm.	The lexical decision task was composed of 270 pairs of stimuli.	MDRS	****
Kalenzaga, 2013⁴⁴	Cross-sectional	AD 22 CG 21	NINCDS-ADRDA	To explore the impairment in patients with AD working self with regard to the affective dimension of AD.	Remember/Know/Guess paradigm following encoding of emotional and neutral words.	MDRS MMSE	****
Kalenzaga, 2013⁴⁵	Cross-sectional	n=40 AD 22 CG 18	NINCDS-ADRDA	To investigate the effect of emotional words encoded with reference to the self on the state of consciousness associated with memory retrieval in AD.	Remember/Know/Guess paradigm following encoding of emotional and neutral words.	MMSE MDRS	****
Kalenzaga, 2014⁴⁶	Cross-sectional	n=33 AD 18 CG 15	NINCDS-ADRDA	To investigate emotional memory enhancement (EME) in AD. And in exploring which memory process (i.e., recollection or familiarity) could be improved by emotional information in the course of the disease.	Remember/Know/Guess paradigm following encoding of emotional and neutral words.	MDRS	****
Kalenzaga, 2016⁴⁷	Cross-sectional	n=155 YA 38 OA 39 VOA 37 AD 41	NINCDS-ADRDA	To introduce some elements concerning positivity effect in aging	Emotional valence rating using an 8-point scale (1 highly negative, 8 highly positive).	MMSE	****
Laisney, 2013⁴⁸	Cross-sectional	16 AD 15 CG	NINCDS-ADRDA	To investigate changes in the cognitive and affective dimensions of ToM in AD	Affective ToM was assessed via a modified version of the Reading the Mind in the Eyes test	Cognitive ToM was assessed by means of preference judgment (PJ) and FB tasks.	*****
Maki, 2013⁴⁹	Cross-sectional	n=54 AD 12 ANC 17 YNC 25	NINCDS-ADRDA	To examine whether recognition of positive facial expressions is preserved in patients with AD	DB99 (Advanced Telecommunications Research Institute International)	CDR	*****
Mograbi, 2012⁵⁰	Cross-sectional	n=43 AD 22 CG 21	DSM-IV-TR	To explore emotional reactivity in mild to moderate AD using film material, investigating the influence of dementia-related material and awareness of condition.	The rating of facial expressions was made with EMFACS, a selective system based on the Facial Action Coding System (FACS).	MMSE, CERAD	****
Mograbi, 2012⁵¹	Cross-sectional	AD 23 CG 21	DSM-IV-TR	To investigate emotional reactions to success or failure in tasks despite unawareness of performance in AD.	The rating of facial expressions was made with EMFACS, a selective system based on the Facial Action Coding System (FACS). and Mann–Whitney U-test.	MMSE, CERAD	*****
Monti, 2010⁵²	Cross-sectional	PRAD 19 HEA 15 HYA 22	NINCDS-ADRDA	To evaluate the efficacy of non-emotional and emotional conflict adaptation mechanisms in healthy young, healthy elderly, and PRAD.	Presentation software Pictures of Facial Affect FACS	CDR	***
Sapey, 2015⁵³	Cross-sectional	n=78 AD 39 HC 39	NINCDS-ADRDA	To better specify the early emotion recognition deficits at mild stages of AD and to disentangle their neuroanatomical correlates.	Facial emotional expression recognition task.	MMSE, CDR	****
Sava, 2017⁵⁴	Cross-sectional	n=63 AD 17 HO 21 HYs 25 n=60 AD 18 HO 21 HYs 21	NINCDS-ADRDA Brain morphology imaging	To compare the memory performance of healthy young and older participants and patients with AD for faces with positive, neutral, and negative emotional expressions in tasks in which memory performance could not be enhanced by familiarity.	Montreal Set of Facial Displays of Emotion	MMSE	*****
Seid, 2012⁵⁷	Cross-sectional	AD 47	NINCDS-ADRDA	To explore the determinants of emotional facial expression in AD and to address the impact of cognitive and neuropsychiatric symptoms, which were considered as potential moderating variables.	International affective picture system (IAPS). The rating of facial expressions was made with EMFACS, a selective system based on the Facial Action Coding System (FACS).	MMSE, GDS, NPI AES	****
Torres, 2015⁵⁸	Longitudinal	AD 30	DSM-IV-TR And NINCDS-ADRDA	To investigate the patterns of change in the ability to recognize emotions in facial expressions among people with mild AD and to explore the sociodemographic and clinical factors that may influence facial emotion recognition in AD over time	The protocol FACES	CDR MMSE	*****
Werheid, 2011⁵⁵	Cross-sectional	AD 18 CG 18	Not reported	To compare patients with mild AD and age-matched healthy adults with respect to performance in a recognition task involving positive, negative, and neutral faces.	Benton Facial Recognition Test PANAS	MEEM CERAD	****

S. No.	Author, Year	Sample	Stimuli and emotions	Tasks	Control tasks	Results
01	Bourgin, 2018⁴¹	AD=16 HOAs=25	The stimuli were 96 color images of natural or manufactured objects, presented against a white background at a visual angle of 9×9.	Saccadic task involving both prosaccades and antisaccades.	An eye-tracking technique during a simple but time-constrained cognitive task	The results suggest that early emotional attention is indeed impaired in AD
02	Daley, 2018³⁹	AD=28 CG = 28 OCs=30	The Advanced Clinical Solutions Social Perception subtest (ACS-SP) to measure emotional perception abilities). Happy, sad, angry, disgusted, afraid, surprised, or neutral.	The Affect Naming task, the Prosody-Face Matching task, and the Prosody-Pair Matching task.	Emotion identification, emotion discrimination, and emotion matching.	The patient group performed significantly worse than control group on measures of cognition and emotional perception.
03	Dourado, 2019⁵⁶	52 participants AD mild n=29 AD moderate n=23	Face drawings Sadness, happiness, anger, or surprise	Matching: instructions–match target face with one of four alternatives; point/verbal response to another example of same emotion and three other expressions. Selection: instructions–point to the sad faces/choose face that matches situation; point response to one of four alternatives.	The subjects must select the target of three other distractors in the same category. Identity discrimination: (same/different emotion). Indicate which of the four drawings best depicts that specific emotion. And indicate the drawing that best described the emotion he had inferred from the stimulus.	Emotional processing difficulties across AD stages. However, when participants needed to recognize the most salient emotion in a situation with evident emotional content, the results suggest that in both groups, there was no influence of cognitive impairment.
04	Duclos, 2018⁴²	n=60 AD 20 HOS 20 HYS 20	The Peter and Mary emotion tasks Battery. Two basic emotions (i.e., anger and surprise), two self-consciousness emotions (i.e., embarrassment and pride), plus the neutral state.	(1) context task, (2) face task, and (3) context–face task	Identification of emotions (What is the emotion expressed by the character?), Discrimination of emotions (Which of the four situations could induce that emotion), Correspondence of emotions (Does the emotion expressed by the character correspond to the context?).	The results suggest that patients with AD have difficulty attributing emotional mental states, and deficits in social norm knowledge and the presence of incongruent information may heighten this difficulty.
05	Giffard, 2009⁴³	AD 26 CG 26	Lists of words (neutral, positive, and negative).	Semantic priming task The lexical decision task.	Identification of words	The results show that this emotional process is preserved in AD and may even help patients to bind semantically close emotional concepts together more tightly.
06	Kalenzaga, 2013⁴⁴	AD 22 CG 21	Two lists of 30 personality trait adjectives were selected from a normalized pool. Paradigms Remember/Know/Guess	Remember/Know/Guess.	The participants were asked to underline the words they recognized from the study list and to indicate whether or not they had a conscious recollection of the learning sequence.	Results indicate that self-reference increased autonoetic consciousness only for emotional and particularly negative trait adjectives.
07	Kalenzaga, 2013⁴⁵	n=40 AD 22 CG 18	Two lists of 30 personality trait adjectives were selected from a normalized pool.	Remember/Know/Guess.	Read aloud, answer questions about yourself, and underline the words you recognized from the list of studies. Report whether or not they had a conscious memory of the learning sequence.	Results for patients with AD show that self-reference increased autonoetic consciousness only for emotional and particularly negative trait adjectives.
08	Kalenzaga, 2014⁴⁶	n=33 AD 18 CG 15	64 nouns/words were divided into four lists of 16 words (i.e., 8 neutral, 4 positive, and 4 negative) matched for frequency, concreteness, and valence.	Remember/Know/Guess	Underline the identified words from the list of studies and indicate whether or not they had a conscious recall of the learning sequence.	Patients with AD were as able as normal controls to benefit from the emotional content of information to improve the recollection of details.
09	Kalenzaga, 2016⁴⁷	n=155 YA 38 OA 39 VOA 37 AD 41	64 nouns/words were divided into four lists of 16 words (i.e., 8 neutral, 4 positive, and 4 negative) matched for frequency, concreteness, and valence.	The task was presented using the SuperLabPro software.	Participants had to read aloud and learn the words, had to generate a sentence containing the word, and after trying four items, the participants had to remember the four words and the corresponding phrases produced.	The results indicated that the positivity bias is most likely to occur in individuals whose cognitive functions are preserved, after long retention delay, and in experimental conditions that do not constrain encoding.
10	Laisney, 2013⁴⁸	AD 16 CG 15	Preference judgment task, False-belief task, and Reading the Mind in the Eyes test	Reading the Mind in the Eyes test	Identification in Matching emotions and Discrimination	We observed impaired performances by patients with AD on all the ToM tasks. However, affective ToM seemed affected to a lesser degree than the cognitive dimension.
11	Maki, 2013⁴⁹	n=54 AD 12 ANC 17 YNC 25	600 colored face images of 6 basic emotional expressions (i.e., happiness, surprise, anger, sadness, fear, and disgust). DB99.	The participants were required to answer by touching the 100% face that corresponded to the expression of intermediate face.	Emotion identification, (What is the emotion expressed by the face/photo on the computer screen?)	In recognition of happiness, there was no difference in sensitivity between YNC and ANC, and between ANC and patients with AD. Patients with AD were less sensitive than ANC in recognition of sadness, surprise, and anger.
12	Mograbi, 2012⁵⁰	n=43 AD 22 CG 21	The groups watched four films, namely, one neutral, one positive, and two negative. Joyful and sad, relaxed and frightened, calm and irritated, and hopeful and hopeless. Joy, surprise, fear, sadness, disgust, anger, and contempt were evaluated.	The groups watched four film excerpts, namely, one neutral, one positive, and two negative.	Self-evaluation (How do you feel after watching this?’). For each emotion, participants were asked to rate how they were feeling.	The study indicates that patients show emotional reactions congruent with stimulus valence, but that subjective reactivity is reduced in comparison with healthy older adults for negative material
13	Mograbi, 2012⁵¹	AD 23 CG 21	Two success–failure computerized paradigms were developed, i.e., one based on reaction time and the other on memory. Frustrated, satisfied; disappointed, satisfied; ashamed, feeling good about himself; and bored, energetic.	Success condition task and one in a failure condition.	Performance evaluation	The results indicated that, relative to controls, patients with AD exhibited impaired awareness of performance, but comparable differential reactivity to failure relative to success tasks, both in terms of self-report and facial expressions.
14	Monti, 2010⁵²	PRAD 19 HE 15 YA 22	Ekman photos: Happy and Fear	The nonemotional conflict task versus emotional conflict task.	Emotion identification, (What is the emotion expressed by the face/photo on the computer screen?)	It was found that, compared to the young adult cohort, the healthy elderly displayed deficits in task-set shielding in the non-emotional but not in the emotional task, whereas PRAD subjects displayed impaired performance in both tasks.
15	Sapey, 2015⁵³	n=78 AD 39 CG 39	Photographs of faces and answer options were displayed on a computer screen. Happiness, anger, disgust, fear, and neutral.	Behavioral tasks, facial gender recognition task, and facial emotional expression recognition task.	Participants were asked to determine whether the face was more feminine or masculine. Participants were asked to select the label that best described the emotional expression	The results indicate that emotion recognition is impaired specifically, rather than as a consequence of global cognitive dysfunction.
16	Sava, 2017⁵⁴	n=63 AD 17 HO 21 HY 25 n=60 AD 18 HO 21 HY 21	The stimuli were 96 black and white photographs (7 cm × 5 cm) with 32 human adult faces against a gray background (each one depicting sad, neutral, and happy emotional expressions). Stimuli were selected from the Montreal Set of Facial Displays of Emotion	Delayed matching-to-sample task, and Emotion classification task.	Identity discrimination: indicate who the same person is. Emotion identification (What is the emotion expressed by the character?)	Results suggest that the positivity effect in memory is not entirely due to the sense of familiarity for smiling faces.
17	Seidl, 2012⁵⁷	47 participants AD	Photos-IAPS: joy, surprise joy, surprise, anger, fear, disgust, sadness, and contempt.	The participants were encouraged to focus their attention on each presented picture (“Let’s have a look at this one”); simultaneously, facial expression was videotaped.	Attentional focus in either emotion-eliciting or neutral images	The result that cognitive deficits are associated with loss of specific facial expression point toward a progressive loss of control of facial expressions, corroborating previous findings.
18	Torres, 2015⁵⁸	AD 30 CG 30	Face drawings Sadness, happiness, anger, or surprise	Tasks of identifying faces, understanding facial emotions, recognizing expression of emotion, and understanding the nature of a situation and the appropriate emotional state that someone would experience in that situation	The subjects must select the target of three other distractors in the same category. Identity discrimination: (same/different emotion). Indicate which of the four drawings best depicts that specific emotion. And indicate the drawing that best described the emotion he had inferred from the stimulus	The findings suggest that people with mild AD have difficulties making emotional interpretations of the environment, mostly due to their worsening global cognition. People with AD had an impaired ability to perceive emotions from situations, particularly when the emotions presented were relatively subtle.
19	Werheid, 2011⁵⁵	AD 18 CG 18	The stimulus material consisted of 192 portraits of Caucasian faces gathered from different databases and selected based on computer-assisted 7-step valence ratings: happy, neutral, and angry	The participants’ task was to decide whether they had previously seen a portrait of the depicted person. Finally, on completion of the task, subjects were asked to fill out the post-test PANAS forms	Identity discrimination: indicate whether same or different person	The pattern of results supports the view that the positivity-induced recognition bias represents a compensatory, gist-based memory process that is applied when item-based recognition fails.

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[TFN1] AD: Alzheimer’s disease; (****) Quality assessment, ADAS-Cog: Assessment Scale–Cognitive Subscale; AES: Apathy Evaluation Scale; ANC: aged normal controls; BDI: Beck Depression Inventory; CDR: Clinical Dementia Rating scale; CERAD: Consortium to establish a registry for Alzheimer’s disease; CG: control group; DSM-IV-TR: Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition; FB: false belief; GDS: Global Deterioration Scale; HC: healthy control; HEA: healthy elderly adults; HO: healthy older; HOAs: healthy older adults; HOS: healthy older individuals; HYA: healthy young adults; HYs: healthy young individuals; IAPS: international affective picture system; MDRS: Mattis Dementia Rating Scale; MMSE: Mini-Mental State Examination; MoCA: Montreal Cognitive Assessment; NINCDS-ADRDA: National Institute of Neurological and Communicative Diseases and Stroke/Alzheimer’s Disease and Related Disorders Association; NPI: Neuropsychiatric Inventory; OA: older adults; OCs: older controls; PANAS: Positive and Negative Affect Schedule; PJ: preference judgment; PRAD: probable Alzheimer’s disease; TMT: Trail Making Test; ToM: Theory of Mind; VOA: very old adults; YA: young adults; YNC: young normal controls.