The main goal of this study was to evaluate the music processing in relation particularly to emotional skill in AD, using a musical protocol including musical skills’ tests (extra-linguistic, Solfeggio and Seashore tests) and a musical emotion recognition test. Thus, we compared the music competences between two groups of patients with AD—MIAD and MoAD—and a control subject group, which they did not significantly differ in gender, laterality, age, educational and musical levels, as well as mood state, but AD patients showed the important cognitive and emotional deficits.
In general, the findings seem to suggest that global weakening of musical processing is a common disorder in AD. The results showed the lower performances of musical competences in AD groups than in the control group, assessing by the extra-linguistic, Solfeggio and Seashore tests.
The extra-linguistic performances were altered in MiAD patients, but it did not significantly decrease over the disease severity. The extra-linguistic aspects (recognition of rhythmic structures, melody memory and recognition of musical timbres) essentially put into play the capacities of working and long-term memory, reflecting the classical results about more important progressive deficit of short-term memory and learning than autobiographical memory [40]. We found the important verbal learning deficit and cognitive impairment in AD groups, though we did not include an auditory working memory test in our study which could have improved our results analysis. Several works have demonstrated that music memory is relatively preserved in patients with moderate to severe AD in spite of otherwise severe overall impairment [16, 17]. However, some reports have described impaired music memory in AD [20, 21, 23]. Besides, several studies have showed that recognition memory was better for the novel sung than spoken lyrics in AD patients [22, 24, 25]. Familiarity of music also is another aspect taken into account to explain the variability of music memory in AD patients [2, 18, 33, 41, 42]. In this sense, the recent study of Slaterry et al. [42] found out that in AD patients, unfamiliar melodies depended more on episodic memory, involving disease-associated activation group differences in precuneus and posterior cingulate cortex, and familiar melodies depended more on semantic memory, involving activation differences in right inferior frontal cortex. In addition, Baird and Samson [18] suggested that perhaps the implicit and procedural memories for musical stimuli remain preserved, but not musical episodic memory. Regarding neural basis, emotion and implicit memory share neural subcortical structures, such as the amygdales or basal ganglia, which are ontogenetically older than those of explicit memories. Furthermore, we found important and progressive deficits of the word lists learning in AD patients, more with the emotionally neutral word list than that with emotionally charged words. We also noted a positive emotional impact of words on learning (emotional memory score) in AD groups, despite the difficulties of memory. However, the emotional effect on learning was less important than that of the control group.
Concerning the Solfeggio test, we observed similar results for note recognition subtest between the participant groups, but not for the note writing subtest. Similar results were found by Sol [39]. This result could be explained in terms of the task difficulty degree. The cognitive competences of the note recognition subtest are similar to those of language recognition tasks, but not for note written subtest. In this last subtest, patients rewrote the name of the note in words on the music sheet instead of drawing it or they randomly placed notes on the music sheet. Nevertheless, we must also consider the praxis, spatial organization or understanding troubles in AD patients, explaining those results, but we did not find a relationship between MMS and Solfeggio scores.
However, we only found a significant correlation between MMS and Seashore scores, which assess essentially basic acoustic changes in music. The performances of the Seashore test progressively decreased from MiAD to MoAD patients, except for pitch interval as others studies have observed, too [10, 43]. The work of Golden et al. [10] also observed an unimpaired sense of pitch interval, but it found a selective deficit of global pitch (melody contour). They suggest that this deficit might be due to auditory working memory deficits and, thus, it might reflect increased demand for coordinated integrative computations between temporo-parietal association cortices vulnerable to AD [44]. The results showed that music aspects of time, rhythm and timbre were more initially resistant to the AD, before dropping to the moderate stage. However, the tonal memory was early altered in the MiAD patients, and then it decreased more in MoAD group. Most of Seashore subtests significantly differentiated the MiAD group from MoAD group, but it did not distinguish the MiAD group from that of the control. The Seashore test would therefore be sensitive to the evolution of the disease, but it could not discriminate effectively the MiAD patients from healthy subjects. In contrast, the extra-linguistic test could distinguish control and MiAD participants, but not between the AD stages. Besides, we found a strong relationship between Seashore and extra-linguistic tests, and so, it lets you choose one of them for evaluations of musical abilities, but taking into account that the extra-linguistic score is composed of more ecological items and faster assessment than those of the Seashore test.
Furthermore, the Seashore and Solfeggio tests showed the strong correlations with the emotional prosody recognition and emotional learning, suggesting that the musical abilities depend on emotional aspects. In our study, emotional prosody can also distinguish control subjects and AD patients, but the most sensitive item to detect MiAD from healthy participants was spontaneous production of intonation. This result suggests the presence of an expressive emotional aprosody from early stage of AD. The similar results were observed by Roberts et al. [45], concerning the early troubles of emotional production, but they also found preserved emotional prosody recognition in patients with AD. Thus, the emotional perceptual aspect would play a more important role in the preservation/impairment of the musical competences than the emotional expressive aspect.
Concerning the musical emotion recognition test, the performances are poorer in AD patients than those of control participants, though the results did not reach to be significantly different between them, despite the cognitive and emotional troubles in the AD groups. Thus, we can observe a trend towards a performance difference between AD and control subjects, though both AD groups showed the similar results. It could also be suggested that processing of musical emotion may be relatively more resistant than other musical skills to AD, as it has previously been observed in other studies [4, 31]. In addition, several studies have also found the similar results using familiar or not familiar music [12, 15, 30, 31]. However, it is necessary to consider a limitation in our work, to the future studies, concerning the small size of items used in this test of musical emotion recognition, because a larger stimulus set with a greater range may have more clearly exposed a deficit. Furthermore, the recognition capacity of musical emotions was not the same for every type of emotion in our study. All participants recognized the joy emotion of music, followed by sadness emotion, but the fear emotion seemed more difficult to recognize from the music pieces by all groups. Fear is a very complex emotional expression and several studies also observed similar results for fear emotion recognition vs. joy and sadness emotions from faces [29, 40, 46]. Recognition impairments for facial expressions of emotion are seen in AD [27, 28] and more altered in semantic dementia. Nevertheless, some studies [4, 46] found unimpaired performances in recognition of non-familiar facial and non-familiar musical emotions in AD.
Moreover, Hsieh et al. [32] observed the common neural substrates supporting the processing of emotions by facial and musical stimuli, involving essentially the right temporal pole, amygdala and insula, but the recognition of musical (but not facial) emotions was also associated with the left anterior and inferior temporal lobe, which are associated with semantics in language. In this sense, the work of Omar et al. [34] observed deficient recognition of emotions from music as well as faces and voices in subjects with frontotemporal lobar degeneration. They observed that the impaired recognition of emotions from music was specifically associated with grey matter loss in a distributed cerebral network including the insula, orbitofrontal cortex, anterior cingulate and medial prefrontal cortex, anterior temporal and more posterior temporal and parietal cortices, amygdala and the subcortical mesolimbic system.
It is also necessary to consider other limitation in our study, concerning the possible semantic associations in some items of musical emotion recognition, for instance, in the case of the fear emotion which can be associated to a movie theme or any other association of an emotion and past experiences. These associations require interactions between musical emotions and music processing. Nevertheless, AD groups showed the important declarative memory troubles. It will be interesting to use a larger item size and to control the semantic associations of musical pieces in future studies analysing musical processing in AD.
Moreover, the preservation/impairment is heterogeneous in the different aspects of musical abilities in AD, essentially due to the diffuse nature of the neural musical network which relies on the participation of the two cerebral hemispheres and in relation to melodic and temporal processing of the functional architecture model by Peretz and Coltheart [47]. The two cerebral hemispheres would be solicited in musical cognition and the preserved or not capacities are indifferent in one or the other. The diffuse nature of the musical neural network would probably be an asset in the relative preservation of certain musical skills. For instance, it is found in the right cerebral hemisphere the time, the timbre, and the joy and sadness recognitions which are mostly preserved at the beginning of the disease. In contrast, the left hemisphere is more responsible for the notions of rhythm, musical reading and the naming and identification of familiar music. This last ability was slightly less affected than other musical skills, maybe due to the relatively good semantic memory and emotional aspect of familiar melodies. We suggested that the emotional perceptive aspect seems to retain certain music skills, which are more resistant than other musical skills to AD. In this sense, several studies have also found an expressive aprosody in the early stages of AD (for review, see [48].