Deficits in emotion processing in Alzheimer’s disease: a systematic reviewABSTRACT
Emotional processing involves the ability of the individual to infer emotional information. There is no consensus about how Alzheimer’s disease (AD) affects emotional processing. Objective: Our aim is to systematically review the impact of AD on emotion processing.
Methods: We conducted a search based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA). The literature search was performed using the electronic databases MEDLINE (PubMed) and Science Citation Index (Institute for Scientific Information [ISI]). The following descriptors were used in the review process: emotion or emotional processing, cognition or cognitive functions, and Alzheimer disease or Alzheimer’s disease. This systematic review was recorded in the International Prospective Register of Systematic Reviews (PROSPERO) under the number CRD42018115891.
Results: We identified 425 articles, 19 of which met our criteria. Visual emotional stimuli were the most used among studies. Most studies used tasks of emotional naming, discrimination, identification, and correspondence. The results were contradictory. Many studies reported that individuals with AD were impaired on emotional perception tasks, while other results reported preserved skills. The relationship between emotional processing and cognition is also unclear. Some studies suggested that general cognitive performance affects performance in emotional perception tasks among people with AD, but other studies have shown deficits in recognizing emotion, regardless of cognitive performance.
Conclusions: Studies are scarce, present contradictory results, and report impairment in emotional processing in relation to cognition. Moreover, the analyses of the correlation between emotion processing and cognitive functioning failed to reveal clear relationships.
Keywords:
Alzheimer’s disease; cognition; emotion
RESUMO
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
INTRODUCTION
Emotion processing refers to the cognitive processes involved in the capacity of understanding other people’s and/or one’s own emotional state.1 Everyday emotions involve a blending of various bottom-up processing of encounters with emotional stimuli along with top-down conceptual knowledge, memories, and linguistic representations.2 Emotional perception may be impaired in healthy aging.3,4,5 Therefore, deficits in emotion processing can be a prominent clinical symptom after acute brain damage, such as traumatic brain injury or stroke, and can be a core feature of the early stages of some neurodegenerative disorders, such as behavioral-variant frontotemporal dementia.6,7,8,9
In the mild stages of Alzheimer’s disease (AD), emotion processing impairments might be relatively subtle and harder to detect.8 People with AD tend to show decreased emotion processing with impaired identification, labeling, matching, and discrimination of emotions.6,7,10,11 Emotion processing has been examined through photos of faces expressing six basic emotions, namely, happiness, sadness, fear, anger, disgust, and surprise.12 Other instruments (i.e., emotional dynamic stimuli such as video clips and movie excerpts) may offer additional information about people with the emotional state of AD. There is some evidence that decreased emotion processing among people with AD may be explained by the structural and functional changes within the frontal and temporal neuronal circuits.13,14 AD pathology, particularly neurofibrillary tangles, initially affects the medial temporal lobe structures, including the entorhinal cortex, hippocampus, and amygdala.15,16 Various studies highlight the essential role of the amygdala in the emotion processing,17,18,19,20 which is supported by neuroimaging studies that show the alterations in the limbic system in people with AD.21,22,23,24 Studies also suggest that people with AD showed impaired emotion recognition, especially for facial expressions.25,26,27,28 However, others have shown that decoding of emotions is comparable in healthy older adults and people with AD.26 In addition, these difficulties do not seem to depend on disease severity.29,30
Specific emotions may vary in their vulnerability to AD pathology. Recent studies indicate that the capacity to identify happiness (i.e., positive emotions) is preserved in AD, while decoding negative emotions seems impaired.16,27,31 The identification of disgust may be preserved,25 while decoding fear is impaired.6,11,25,27,32,33,34 There are controversies about people with AD ability to recognizesadness, anger, and surprise11,27,34,35. Therefore, we may assume that in AD, the emotion processing is differently affected, and that the identification of some specific emotions may be impacted, while others are not.
Although it was not consistently demonstrated throughout the literature,6,10,36 some authors also suggested that the observed impairment of emotion processing tasks in AD is not necessarily related to impaired emotional decoding abilities, but may, in fact, occur secondary to generalized global cognitive decline.1,13,34,37,38 However, other authors did not obtain the same results and concluded that people with AD may present impaired emotional recognition per se. Thus, given the current controversial results about the impairment of emotion processing in AD, we hypothesized that people with AD may have an impaired capacity of processing emotional information even in the mild stages of the disease. Deficits in emotion processing have been associated with negative caregiver outcomes39 and functional disability8 in AD. Therefore, in this systematic review, we aimed to better understand the extent to which emotion processing is impaired in people with AD.
METHODS
This systematic review has been performed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA). We searched the Thomson Reuters Web of Science (Institute for Scientific Information – ISI) and MEDLINE (PubMed), including articles published from January 1, 2009, and November 11, 2019, in English, which presented studies with cross-sectional or longitudinal designs about the relationship between emotion processing and cognition among people with AD.
We applied the key words “emotion,” “emotional processing,” “cognition,” and “Alzheimer’s disease” in different combinations for each database. For MEDLINE (PubMed), we applied the following combinations: (emotional processing OR emotional [MeSH Terms] OR emotion [MeSH Terms]) AND (alzheimer disease OR alzheimer’s disease [MeSH Terms]) AND (cognition AND cognitive functions [MeSH Terms]), with the following filters: Humans, English, and Publication Date from 2009/01/01 to 2019/11/01.
For the identification of articles in the Thomson Reuters Web of Science (ISI), we applied the following search strategy: #1 (TS=(alzheimer disease OR alzheimer’s disease) #2 (TS=(emotion OR emotional processing) #3 (TS=(cognition OR cognitive functions OR cognitive functioning) #3 AND #2 AND #. We also applied the following filters: Language: English; types of documents: articles; and date range: 2009–2019. The exclusion criteria included systematic reviews, meta-analysis, articles with no casuistic, and case reports or studies about emotion processing and cognition in other diseases. Initial article-screening was performed by two authors via abstract review. We excluded articles that clearly did not fulfill the inclusion criteria, and we maintained the ones that were possibly eligible. When there was not a consensus among the two authors, the article remained as potentially eligible and was included in the next assessment of eligibility. Disagreement between both authors was solved by an independent author.
The selected articles from the first phase were read by two independent authors to adjust eligibility. In this phase, the main exclusion criteria for each study were registered in the PRISMA flowchart (Figure 1) to compose the flow of article selection.
To maintain the standard suggested by the PRISMA method, this systematic review was registered in the International Prospective Register of Ongoing Systematic Reviews (PROSPERO) as CRD42018115891.
All the included articles were submitted to the Mixed Methods Appraisal Tool version 2018,40 a tool of critical assessment that evaluates the quality of empirical studies.
RESULTS
We found 425 articles, 182 on the ISI database and 243 on PubMed/MEDLINE. After excluding the cross-references (n=42), we selected 383 articles. The excluded articles (n=364) were selected and analyzed according to the eligibility criteria. The exclusion flowchart of selected articles is described in Figure 1.
We included the complete version of the remaining 19 articles. The selected articles were fully accessed and independently organized as shown in Table 1 that contained the following information: author/year, design, sample, operationalization of AD diagnosis, objective, emotional processing evaluation, cognitive evaluation, and quality assessment.
Sample
From the 19 articles analyzed in this review, 16 studies compared AD with a control group.39,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55 One study assessed people with AD in mild and moderate stages.56 Seidl et al.57 assessed one group of 47 individuals with AD, but they did not specify the stage of disease severity. In Torres et al.,58 the comparison was performed in two different moments of people with mild AD.
Operationalization of Alzheimer’s disease diagnosis
Diagnoses of possible or probable AD in 13 studies were made according to the criteria of the National Institute of Neurological and Communicative Disorders and Stroke and the Alzheimer’s Disease and Related Disorders Association (NINCDS/ADRDA)39,41,42,43,44,45,46,47,48,49,52,53,54,57 or based on the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV) guidelines.50,51,56,58 Computed tomography and/or magnetic resonance imaging examinations were occasionally used to support the diagnosis.41,48,53,54,56,58 The specific diagnostic criteria used to identify possible or probable AD were unclear in one study.55
Degree of severity in Alzheimer’s disease
Of the 19 studies, 8 studies analyzed the impairment in patients with AD at mild and moderate levels,42,43,46,47,48,50,51,56 5 studies evaluated individuals with mild AD,49,53,54,55,58 and 6 studies did not measure staging or the severity of the disease in the participants of the AD group.39,41,44,45,52,57
ASSESSMENT CRITERIA
Tasks with various visual stimuli were most frequently applied. In 14 studies, images or drawings were applied.39,41,42,48,49,50,51,52,53,54,55,56,57,58 Images of facial expressions in black and white were applied in three studies.52,54,55 Color images of natural or manufactured objects were applied in three studies.41,48,49 Two studies applied movies42,50 using movie excerpts and a short black-and-white video. Finally, one study51 also applied two computerized paradigms of success–failure manipulation.
The five remaining studies used a word list as a stimulus.43,44,45,46,47 The words in word lists were classified as positive, negative, and neutral,43,47 as well as adjective lists related to personality traits44,45 and noun lists standardized by Bonin et al.46,59 in which the words were classified according to emotional state using a 5-point scale from 1 as “very unpleasant” to 5 as “very pleasant.”
From the 19 studies, 9 studies analyzed the following basic emotions: happiness, surprise, anger, sadness, fear, and disgust. Four studies included facial expressions of fear,39,49,52,53 and the facial expression of surprise was investigated in five studies.39,42,49,56,58 Only three studies analyzed the recognition of facial expressions of disgust,39,49,53 and four studies39,53,54,55 also included neutral expressions. Dynamic emotional stimuli such as video clips and short movie excerpts were used to assess the emotional processing in two studies.42,50
TASKS FOR ASSESSMENT
The assessment tasks were frequently divided into complementing stages according to the level of required cognitive effort. These stages were frequently identified in the studies as emotion identification, discrimination, selection, and correspondence of emotions. These procedures assess various cognitive competences and are considered the first step of emotion processing impairment analysis. Table 2 shows a summary of the specific tasks used in each initial study and includes the main results.
Results of assessment tasks
In eight studies,39,48,49,52,53,54,55,57 photos were used as stimuli, and the participants were invited to select the frame, which best described the emotional expression represented. No significant difference in performance was observed among healthy older adults and people with AD in two studies.49,54 The other six studies concluded that people with AD had worse performance than the control group, and only one study52 related the worse performance to the specific decline in emotion processing. Werheid et al.55 attributed the deficit to memory impairment in AD. The other four studies explained the worse performance of people with AD in more specific neurodegenerative processes in the amygdala and hippocampus and in the general progression of the disease.39,48,53,57
Dourado et al.56 and Torres et al.58 utilized the FACES protocol, which consists of four increasingly difficult facial recognition tasks. The first task investigated the visuoperceptual capacity of identifying faces. The second task examined the comprehension of facial emotions. The third task examined if people with AD can conceptually recognize the emotional expression, and the fourth, the most complex task, assessed the capacity of understanding the emotional nature of one situation. In the study of Dourado et al.,56 the results of task 1 have shown a relationship between the impairment of visuoperceptual capacity to identify faces and decreased performance related to cognitive competence. No differences between mild and moderate AD were observed in task 3. No clinical variables predicted the performance in task 4 among people with mild AD, even after the adjustment to the severity of cognitive decline; however, among people with moderate AD, there was a relationship between task 4 and the emotional recognition domain of awareness of the disease. In the baseline assessment of the study of Torres et al.,58 there was no relationship between tasks 1, 2, 3, or 4 and the clinical variables. No relation was observed between the global score of FACES and the sociodemographic or clinical variables. After 6 months, the study has shown a significant difference between both assessments on the scores of task 4. These results show that the emotional impairment in the mild stage of the disease is related to the cognitive impairment and with the progression of AD. However, the study had a small sample and a time span of only 6 months.
To determine the impact of emotion information in early attentional processes among people with AD, Bourgin et al.41 applied an eye-screening paradigm and a task that mixed prosaccades and antisaccades with the emotional stimulus. The results suggested that people with AD had difficulties in rapidly and automatically focusing their attention on the emotional characteristics of the faces.
Two studies42,50 used video clips as stimuli to assess the capacity of people with AD on the discrimination and tagging of emotions. Duclos et al.42 used the Peter and Mary test, which is composed of short videos with black-and-white images, without sound, and with two characters. This study also applied images with colorful drawings that represented several activities of daily living. The results demonstrated that people with AD had impairment in decoding emotional mental states of facial expressions.
Mograbi et al.50 applied movie excerpts, one neutral, one positive, and two negatives to investigate the influence among people with mild and moderate AD. The results showed that the participants demonstrated reduced reactivity to negative movies, but they exhibited a pattern of facial expressions similar to the control group in all other movie excerpts. Mograbi et al.51 investigated the emotional reactivity to success or failure among people with AD in comparison with a cognitive healthy control group. The study applied two experimental computerized paradigms of manipulation of success and failure, i.e., one based on reaction time and the other on memory. The results of the group of people with AD have shown a reduction in the awareness about the performance, with difficulties to discriminate between the success and failure conditions. In contrast, they have shown the same levels of emotional reactivity of the control group in both experiences.
Five studies43,44,45,46,47 used word lists classified according to the emotional valence as the stimulus. Kalenzaga et al.47 reported that people with AD have shown bias toward positive stimuli, especially in the recognition task after the semantic processing instruction, while, in the group of healthy older adults, the positive preference was observed in both recovering tasks. In the study of Kalenzaga et al.,46 both people with AD and cognitive healthy controls may have benefited from the emotional content of the information, with better performance in the retrieval of the information. People with AD were as able as normal controls to benefit from the emotional content of information to improve the recollection of details.
One study44 showed that although people with AD had an explicit view of themselves, they only pointed out negative characteristics. Another study45 showed that people with AD produced fewer correct answers when compared with cognitive healthy controls. The data confirm that, in AD, there is a specific impairment in autonoetic awareness and show that declarative memory impairment, which is the characteristic of AD pathology, is mainly an impairment in episodic memory. When a lexical decision task was applied43 by comparing the automatic semantic effects between people with AD and cognitive healthy control group, the results reveal that in both groups, there were primary semantic effects to neutral concepts, but they were decreased in comparison with those effects to emotional concepts, especially negative ones. These results have shown that the emotional processing is preserved in AD and can even help people with AD to reconnect to the emotional semantic concepts.
Results of the emotional valence assessment tasks
The eight studies that assessed emotional valence (i.e., positive, negative, and neutral)41,43,44,45,46,47,50,51 had differing results. In the study by Bourgin et al.,41 people with AD did not show differences in relation to the emotional category in any of the tasks. These results suggest that the early emotional attention is impaired among people with AD.
The analysis of Kalenzaga et al.46 indicated that, compared with the control participants who have recognized both emotional and neutral words, people with AD recognized more neutral than emotional words. This result is in accordance with the studies that reported that people with AD did not retrieve emotional items better than they retrieve the neutral ones.60,61,62 In the study of Kalenzaga et al.,47 there was a significant effect of emotional valence, indicating that participants remembered more positive than neutral words. The results suggested that the positivity bias is presented only if the memory performance scores have a certain pattern.
In the study of Mograbi et al.,51 there were no significant differences among the groups in the positive and negative tasks. Therefore, the affective valence of the failure experience is processed even though there is no awareness about the task performance. In the experiment with movie excerpts, Mograbi et al.50 found that participants of the AD group may have impairments in self-reported reactivity to negative stimuli. All of the emotions and general reactivity were significant, with more positive emotional changes in response to the positive excerpt and negative alteration in the two negative excerpts.
Three studies have shown different results in comparison with the previous ones, which show a more significant effect of the positive emotional valence among people with AD and controls. Giffard et al.43 showed a facilitating effect of the supplementary emotional component in the semantic processing. The primary semantic effects were higher to the negative concepts than to the neutral and positive ones.
The study of Kalenzaga et al.44 indicated that, in comparison with other encodings, the negative valence is salient to the self-reference of people with AD. Previous studies that explore the effect of valence on emotional processing show that the information remembered about oneself is generally related to the positive valence.63,64
In the results of Kalenzaga et al.,45 while investigating the interaction between the decoding condition and the emotional valence, there was a contrasting pattern of performance. Only the negative valence had a significant effect on the autonomous awareness of people with AD in the condition of self-reference. However, the self-reference effect was also marginally significant to the adjectives of positive characteristics, and pairwise comparisons have shown that there was no significant difference between the answer rate to positive and negative adjectives.
Findings of studies about cognitive impairment an emotion processing in Alzheimer’s disease
Seid et al.57 suggested that cognitive changes influence the recognition of facial expressions. The study of Bourgin et al.41 agreed with this point as it reported that people with AD had difficulties in quickly and automatically focusing their attention on the emotional features of faces. Other studies39,42,48,52,53 have also identified that cognitive impairment and disease severity are related to deficits in the recognition of facial expression, particularly in more complex tasks that supposedly would require more cognitive resources. In agreement, some studies56,58 suggest that difficulties in recognizing emotions are more prevalent in relation to more subtle emotions among individuals with AD.
However, the study of Werheid et al.55 suggested that the emotion-based aspects of old/new decisions for faces are preserved in people with mild AD. Gifard et al.43 and Sava et al.54 showed that emotional processing is preserved in AD and may even help people with AD to link semantically close emotional concepts more tightly. These results are in line with previous findings showing no difference in facial emotional expression processing between healthy older participants and participants of the AD group,35,65 especially for faces with happy expressions.49
The results shown by Kalenzaga et al.46 corroborate the findings of previous studies44,45 and confirm that people with AD have a specific deficit in the episodic component of memory for words. Furthermore, Kalenzaga et al.47 indicated that the positivity bias is most likely to occur in individuals whose cognitive functions are preserved, after a long retention delay, and in experimental conditions that do not constrain encoding.
Mograbi et al.50 showed that people with AD showed emotional reactions congruent with stimulus valence, but the subjective reactivity is reduced in comparison with healthy older adults for negative material. Mograbi et al.51 indicated a dissociation between impaired performance judgment and preserved emotional reactivity to failure in AD.
DISCUSSION
To better understand the impairment in emotion processing in people with AD, this systematic review analyzed 19 studies. The main findings suggest the following: (1) people with AD may have impairments in the ability to process emotions, but there are controversies about the beginning of emotion perception impairment among them, (2) there is not a methodological standard in the assessment of emotion processing, which may influence the results and contribute to a variability and lack of consistency of findings in the area, (3) the studies disagree whether the impairment in emotion processing is related to global cognitive impairment or to a decrease in a more specific system of emotion processing, (4) the impairment in emotion processing may be independent of stimulus or task used in the testing of various emotional aspects, (5) there are discrepancies in identifying emotions; while some studies showed that the emotions with negative valence may be more impaired than the positive emotions, other studies reported that the degree of this impairment may be influenced by disease severity and level of excitement (e.g., anger elicits more excitement and is better perceived than sadness), and (6) the analysis of the effect of emotional valence has shown influence on cognitive performance among people with AD.
The beginning of emotion processing impairment among people with Alzheimer’s disease
The beginning of emotion processing impairment among people with AD has not been discussed enough in any of the evaluated studies. There is almost a consensus that the abilities of emotion perception are frequently impaired even among people with mild dementia due to the impairment of limbic system.66,67,68,69 Therefore, the neurodegenerative process among people with AD may be responsible for increased impairment in emotion perception.70,71 However, some studies consider that the emotion processes are relatively preserved in mild dementia, in comparison with other cognitive domains, such as semantic memory.35,37 Other studies also support that people with AD may retain the capacity of understanding the emotion, independently of the decrease in the cognitive capacity, and they remain capable of being involved in nonverbal communication that may occur in their interpersonal relationships.72 Nonetheless, only the study reported by Giffard et al.43 suggested that emotion processing is relatively preserved in mild dementia, in comparison with other cognitive domains. Conversely, some studies39,42,48,50,52,53,56,58 point out that the impairment of emotion processing may start even in the mild cases of AD due to the cognitive impairment.
We may observe that the results of the reviewed studies highlight the beginning of the impairment of emotion processing in different stages of the disease. However, these discrepancies among studies may be a result of the variability of objectives and different study methodologies, which may influence and hinder the process of identifying the key points. In addition, the complexity of tasks suggests multiple steps/components that could result in failures/low scores, some of which may not be related to the core features of emotional processing. For example, failed naming of emotions based on face stimuli could be tied to emotion processing/recognition or language disruption in semantic networks. Therefore, more longitudinal studies are necessary to identify the exact stage of the disease in which those difficulties occur. Identifying earlier this kind of impairment would be crucial to a differential diagnosis and to the development of strategies of intervention to facilitate communication and emotional expression of people with AD.
Performance in emotional processing in individuals with Alzheimer’s disease
Most studies used traditional methods (i.e., naming of emotions, discrimination, identification, and correspondence) that have been used in the last decade to assess emotion processing. Due to the cognitive competences involved in each of these different procedures, it is understood that the implicit cognitive processes involved in each task may be affected by the disease. Thus, we may highlight that there is not a consensus about the impairment involved in the capacity of decoding emotions among people with AD, as some results show that there are abilities preserved in AD, while others report deficits in this ability. Maybe, these controversies are caused by the variability of stimuli used in the assessment. This diversity may produce bias or inconsistency of results that are sometimes contradictory. For example, Laisney et al.48 reported that people with AD may have more difficulties in tasks that involve various cognitive domains, such as language, verbal working memory, and social cognition, in comparison with their difficulties in affective tasks. In contrast, Bourgin et al.41 suggest that the early emotional attention is impaired among people with AD in a technique of sight-screening during a simple cognitive task. Overall, the results have been generally attributed to the characteristic decline in AD. However, we may consider that the lack of standardization of assessment instruments to consistently investigate whether people with AD maintain their preserved capacity of recognition of others emotions as well as the lack of expression of their own emotions may be directly related to their performance.
Capacity of perceiving emotions
In relation to specific emotions involved in the decoding tasks, some studies investigated the ability to identify specific emotions such as happiness or sadness. Previous findings31,35,73,74 highlight that the capacity to process some emotions is preserved in AD (e.g., happiness and disgust). Other studies highlight that the participants have particular impairment in the decoding of emotions, such as fear.6,25,75 There is contrasting evidence using a longitudinal design to assess the recognition of facial expressions among people with AD. A study58 reported that the participants continued to appropriately recognize the basic emotions represented in simple drawings but had more difficulties in a more complex task (i.e., identifying the emotional state that would be experimented in a particular situation). However, the results of Sapey-Triomphe et al.53 in a cross-sectional design showed that people with AD were impaired in the recognition of each one of the various basic emotions (i.e., anger, fear, happiness, and, on a lower degree, disgust). The decline in the ability of emotional decoding was significantly related in AD to all types of emotions. There are assumptions that the performance in the recognition of emotions is related to the volume of expected brain structures. However, the performance on the recognition of emotions was negatively related to the majority of volumes in the gray matter in the interest regions. In particular, the performance in recognition of fear was negatively related to the amygdala volume.53 These data contradict other studies76,77 that associated the amygdala function in the processing of fear. Various studies highlight the central role of the amygdala in the emotion processing17,19,20,78 and support the hypothesis that the amygdala is involved in the process of the response of the stimuli to several emotions, which may explain why the decline in the emotional coding of people with AD is not restricted to one specific emotion such as fear.79 It is reasonable to consider that the impact of the neurodegenerative process associated with AD may affect the identification of specific emotions. This point may indicate that regional involvement in each kind of emotion recognition follows distinct patterns, which supports the localizationist view that postulates unique regional networks for each emotion.17 Due to the progressive nature of AD, longitudinal studies with the support of neuroimaging could provide more comprehension of the change patterns in the process of discrimination of emotions among people with AD.
Relationship between emotion processing and cognitive domains
The relationship between deficits in emotion processing and cognitive functioning in people with AD is still underestimated. Although decline in emotion perception may occur, the impact of the global cognitive decline associated with AD across studies varies. Some studies suggest that global cognitive performance affects the performance on tasks of emotion perception among people with AD, but other studies show a decline in the recognition of emotion, independently of the cognitive performance. We hypothesized that these results may be due to the considerable heterogeneity of methods and assessment of cognitive and emotional processes.
Few studies investigate the relationship between cognitive impairment, the severity of the disease, and the impact on the perception of emotions.53,56,58 Moreover, some authors support that emotion processing impairment exists independently of disease severity. Various tools have been used to assess cognitive functions among people with AD. However, most studies have applied the MMSE to assess the association between cognitive state and emotion processing in tasks and procedures. The emotion decoding performance in AD was significantly related to MMSE scores, but some studies did not find this significant relation. Therefore, the strength of these results may be cautiously considered since the MMSE is a tool for screening cognitive decline, susceptible to education and socioeconomic status. Studies that only include screening tests may have limited validity in their findings. A comprehensive neuropsychological assessment of different cognitive domains would have more power to disentangle, in which cognitive functions are more or less related to the emotional processing in AD. Thus, we may consider that the relationship between emotion processing and global cognitive capacity is not clear.
The effect of different emotions in Alzheimer’s disease
The research about emotional valence and its impact on emotion and cognitive processing in AD has been explored, and the results are inconsistent. Some studies have shown the existence of a positive bias.46,47,49,55 For example, the study of Werheid et al.55 shows that the positive bias is really present and affects the performance of people with AD, as well as in cognitive healthy old adults. These data represent evidence of preservation of emotion processing in people with AD. However, we may highlight that the results of studies have shown significant difference among assessed groups, and, therefore, we may consider that, in general, there is a decline in the cognitive capacities of processing emotions and responding to them.
Our study has some limitations that should be considered. There are a limited number of studies that investigate emotional processing in AD, and many of them have low statistical power. In addition, the variety of objectives and methodologies in the reviewed studies hinder the identification of key points. More research is necessary, therefore, to establish the attributions of emotions in relation to cognition.
Our main target was to analyze the relationship between emotion processing and cognition in mild and moderate AD. We concluded that there is evidence that suggests the presence of emotion processing deficits even among people with mild AD. However, the relationship between emotion processing and cognition is not clear. The existing literature presents contradicting results and reports emotion processing impairment in relation to cognition but does not discuss the possible implications of this impairment in social (dys)function. Crucially, emotion processing impairment may negatively impact the well-being of people with AD and their caregivers, which could be an important discussion for future studies.
More longitudinal studies are necessary to investigate the relationship between cognition and emotion processing during the disease progression. Potentially confusing factors such as global cognitive decline, presence of neuropsychiatric symptoms, and mood must be observed. Studies that include neuroimaging data, such as volumetric analyses of the amygdala, may also enhance the comprehension of the processes involved in emotion recognition among people with AD. Therefore, the progressive neuropathological alterations that characterize the disease may impact on emotion processing, and a sensitive focus on this process may help to refine interventions that encompass social interaction.
ACKNOWLEDGMENTS
The authors thank Dr Sara Mason and Dr Shelley Peery, from the Research and Editing Consulting Program (RECP) coordinated by Prof. Mary Beth Spitznagel, associate professor of the Department of Psychological Sciences of the Kent State University, for the careful revision of the manuscript and editing for English language.
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1
This study was conducted by the.Center for Alzheimer’s Disease, Institute of Psychiatry, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil.
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Funding: Marcia Cristina Nascimento Dourado is a researcher funded by the National Council for Scientific and Technological Development — CNPq, crant number 304461/2020-2
