Selective Impairment of Musical Emotion Recognition in AD and aMCI Patients

Selective Impairment of Musical Emotion Recognition in Patients with Amnesic Mild Cognitive Impairment and Mild to Moderate Alzheimer Disease

Introduction
Alzheimer’s disease (AD) and amnesic mild cognitive impairment (aMCI) are significant neurodegenerative conditions that profoundly affect cognitive and emotional processing. AD, the most common form of dementia, is characterized by memory loss, executive dysfunction, and various neuropsychiatric symptoms such as apathy, depression, and anxiety. aMCI, on the other hand, represents an intermediate stage between normal aging and dementia, with a high risk of progression to AD. Both conditions are associated with deficits in emotion recognition, particularly for negative emotions like fear, anger, and sadness. However, the ability of patients with AD and aMCI to recognize emotions conveyed through music remains less understood. This study aimed to investigate whether musical emotion recognition is impaired or retained in patients with AD and aMCI, and to explore the relationship between this ability and cognitive function.

Background and Significance
Music is a universal medium of emotional expression and cultural identity, capable of evoking strong emotional responses. Previous research has shown that music can reduce anxiety, improve behavioral symptoms, and enhance autobiographical memory recall in patients with dementia. Studies on facial and vocal emotion recognition in AD and aMCI have consistently reported deficits in processing negative emotions, while the recognition of positive emotions like happiness remains relatively intact. However, findings on auditory emotion recognition, particularly through prosody, have been inconsistent. Some studies suggest that patients with AD struggle to recognize emotions from prosody, while others report no significant impairment. This discrepancy highlights the need for further research into non-verbal auditory emotion recognition, such as through music, which may provide a purer measure of emotional processing without the confounding influence of verbal semantics.

Musical emotion recognition involves a distributed cerebral network, including the amygdala, hippocampus, orbitofrontal and temporal cortices, and anterior cingulate. These regions are critical for emotional processing and are often damaged in AD. Interestingly, musical memory appears to be preserved in AD, suggesting that musical emotion recognition may be dissociated from musical memory. This study hypothesized that patients with AD and aMCI would exhibit impaired recognition of musical emotions, particularly negative emotions like fear, and that this impairment would correlate with cognitive decline.

Methods
The study recruited 16 patients with AD, 19 patients with aMCI, and 16 healthy controls (HCs) from the First Affiliated Hospital of Anhui Medical University between March 2015 and January 2017. All participants underwent standardized neuropsychological assessments, including the Mini-Mental State Examination (MMSE), to evaluate general cognitive function. Patients with aMCI were diagnosed based on Petersen’s criteria, while AD diagnoses followed the National Institute of Neurological and Communicative Disorders and Stroke and the Alzheimer’s Disease and Related Disorders Association (NINCDS-ADRDA) criteria. Exclusion criteria included hearing or visual impairments, inability to comprehend task instructions, and significant neurological or systemic illnesses.

The musical emotion recognition test involved 40 instrumental musical excerpts designed to evoke happiness, peacefulness, sadness, and fear. Participants were required to match each excerpt to one of the four emotional labels. The primary measure was the accuracy of identifying each emotion type. Statistical analyses included one-way ANOVA to compare emotion recognition scores among the three groups, MANOVA to explore group differences within each emotion category, and Pearson’s correlation analysis to examine the relationship between MMSE scores and musical emotion recognition.

Results
Demographic and neuropsychological characteristics of the participants showed no significant differences in age, gender, or education level among the three groups. However, MMSE scores were significantly lower in the AD and aMCI groups compared to the HC group, indicating cognitive decline in the patient groups.

The results revealed a significant impairment in the recognition of fearful musical emotions in both the AD and aMCI groups compared to the HC group. The mean recognition scores for fearful emotions were 7.88 ± 1.36 for HCs, 5.05 ± 2.34 for aMCI patients, and 3.69 ± 2.02 for AD patients. A one-way ANOVA confirmed a significant main effect of group (F(2,50) = 18.70, P < 0.001). Post-hoc analysis indicated that both patient groups performed worse than HCs in recognizing fearful emotions, with no significant difference between the AD and aMCI groups. In contrast, there were no significant differences among the three groups in recognizing happy, peaceful, or sad musical emotions.

MANOVA further supported these findings, showing a significant overall group difference (Hotelling’s trace; F(9,90) = 2.857, P < 0.001) and significant group differences in the recognition of fearful emotions (F(2,48) = 18.703, P < 0.001). No significant group differences were found for the other emotions.

Correlation analysis demonstrated a significant positive relationship between MMSE scores and the recognition of fearful musical emotions in patients with AD and aMCI (r = 0.578, P < 0.001). This suggests that cognitive function plays a crucial role in processing fearful emotions. However, no significant correlations were found between MMSE scores and the recognition of happy, peaceful, or sad emotions.

Discussion
The study’s findings indicate that patients with AD and aMCI exhibit selective impairment in recognizing fearful musical emotions, while their ability to recognize happy, peaceful, and sad emotions remains relatively intact. This selective deficit aligns with previous research on facial and vocal emotion recognition in these patient populations, which also reported impairments in processing negative emotions. The amygdala, a key structure for processing fear, is often damaged in AD, which may explain the observed deficits in recognizing fearful musical emotions.

The preservation of happy emotion recognition in patients with AD and aMCI may be due to the involvement of different neural substrates, such as the basal ganglia and ventral striatum, which are associated with positive emotions. Additionally, the structural variability of fearful stimuli, which often include dissonance and irregularity, may make them more challenging to recognize than other emotions.

The positive correlation between MMSE scores and the recognition of fearful emotions suggests that cognitive decline contributes to the impairment in processing negative emotions. This finding underscores the importance of maintaining cognitive function for emotional processing in neurodegenerative diseases.

Limitations and Future Directions
This study has several limitations. First, the sample size was relatively small, which may limit the generalizability of the findings. Second, the study did not include functional neuroimaging to directly correlate the observed deficits with specific neural structures. Future research should combine musical emotion recognition tests with fMRI to explore the neural basis of these deficits in greater detail. Additionally, longitudinal studies could provide insights into the progression of emotion recognition impairments as AD and aMCI advance.

Conclusion
In conclusion, this study provides evidence of selective impairment in recognizing fearful musical emotions in patients with AD and aMCI, while the recognition of other emotions remains preserved. This impairment is likely related to the degeneration of the amygdala and other critical neural structures involved in processing negative emotions. The findings highlight the importance of considering emotional processing in the diagnosis and management of neurodegenerative diseases and suggest that musical emotion recognition tests could be a valuable tool for assessing emotional deficits in these patients.

doi.org/10.1097/CM9.0000000000000460

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