Music and prosody after traumatic brain injury
Perception of music and speech prosody after severe Traumatic Brain Injury
Running Head: Music and prosody after traumatic brain injury
Laurène Léard-Schneider1 & Yohana Lévêque1,2
1 Institut des Sciences et Techniques de la Réadaptation (ISTR), University Claude Bernard Lyon I, Lyon,
France
2 Lyon Neuroscience Research Center, INSERM & CNRS, University Claude Bernard Lyon I, Lyon, France
1 Music and prosody after traumatic brain injury
Abstract
The present study aimed to examine the perception of music and prosody in patients who had undergone a severe
Traumatic Brain Injury (TBI). Our second objective was to describe the association between music and prosody impairments in clinical individual presentations. Thirty-six patients who were out of the acute phase underwent a set of music and prosody tests: two sub-tests of the Montreal Battery for Evaluation of Amusia evaluating respectively melody (scale) and rhythm perception, two sub-tests of the Montreal Evaluation of Communication on prosody understanding in sentences, and two other tests evaluating prosody understanding in vowels. Forty- two percent of the patients were impaired in the melodic test, 51% were impaired in the rhythmic test and 71% were impaired in at least one of the four prosody tests. The amusic patients performed significantly worse than non-amusics on the four prosody tests. This descriptive study shows for the first time the high prevalence of music deficits after severe TBI. It also suggests associations between prosody and music impairments, as well as between linguistic and emotional prosody impairments. Causes of these impairments remain to be explored.
Key-words: emotion perception – acquired amusia – intonation processing – auditory cognition – nonverbal information
2 Music and prosody after traumatic brain injury
Introduction
Traumatic brain injury (TBI) is a complex syndrome associated with multiple pathophysiological mechanisms and multisystem damage. After a patient with severe TBI regains consciousness, cognitive (Rabinowitz & Levin,
2014), behavioral (Stéfan & Mathé, 2016), and emotional impairments (Panayiotou, Jackson & Crowe, 2009;
Gouick & Gentleman, 2004) become apparent over time along with physical impairments which are the primary focus of rehabilitation. These impairments severely reduce patients’ social and professional integration. Despite vast clinical heterogeneity, recurrent symptoms at follow-up have been described. In particular, patients’ communication and social skills are frequently altered and recover poorly (Thomsen et al., 1984; Brooks et al.,
1986; Ietswaart et al., 2008). The interpretation of nonverbal information in communication is typically impaired
(Bosco et al., 2017), including decoding the emotional state of others (Milders et al., 2008). This deficit in emotion recognition likely contributes to the impairment in social skills. Emotion recognition was correlated to relationship well-being in stroke patients (Blonder et al., 2012, Leung et al., 2017). Injured patients with social skill deficits often display facial and vocal emotion recognition deficits as well (Dimoska et al., 2010). Both deficits are present shortly after a brain injury, which rules out the hypothesis that social skill deficits are caused by environmental or mood changes (Ietswaart et al., 2008).
At the neurological level, the cerebral regions which are the most frequently and severely damaged are part of networks underlying emotion perception: the frontal and temporal areas as well as the limbic system (Umile et al., 2002; Levine et al., 2013; Phillips et al., 2003; Drapeau et al., 2011). A deficit in emotion perception has been linked to TBI severity (Rosenberg et al., 2015), the degree of frontal or fronto-temporal functioning
(Martins et al., 2012; Spikman et al., 2012) as well as to the sex of the patient, with weaker emotion recognition in males than females after TBI (Rigon et al., 2016).
In the auditory domain, several studies have provided evidence for a deficit in emotional prosody perception, reflected by patients’ difficulty in recognizing emotions expressed in speech when no semantic cues are available
(Dimoska et al., 2010; Ilie et al., 2017; McDonalds & Saunders, 2005; Zupan et al., 2014). Whether the impairment extends to non-emotional prosody, i.e., linguistic distinctions such as interrogative versus declarative intonation, is not clear. Ietswaart et al. (2008) did not find any impairment in this area, while Milders et al.
(2003) did report impairment, a discrepancy that might be explained by the higher average severity of TBI in
Milders et al.’s study.
3 Music and prosody after traumatic brain injury
To our knowledge, only two studies have investigated music perception in TBI patients. Balzani et al. (2014) reported frequent rhythmic impairment and a decrease in subjective musical pleasure in a sample of 10 mild TBI patients, while melody discrimination and production were preserved. Drapeau et al. (2017) did not find a deficit in musical emotion categorization or in the discrimination of same or different musical pairs in a sample of 20 mild TBI and 10 severe TBI patients. Links between prosodic and musical abilities have still been suggested in different populations. Congenital amusic individuals, who present deficits in pitch processing and musical short- term memory, also show subtle prosody deficits in perception (Stewart, 2008; Patel et al., 2008; Liu et al., 2010;
Lolli et al., 2015; Thompson et al., 2012; Pralus et al., 2019). Musical expertise through formal instrumental training enhances the ability to recognize emotions in speech prosody (Lima & Castro, 2011). Cerebral correlates of prosody processing (Schirmer & Kotz, 2006; Belyk & Brown, 2014; Frühholz et al., 2015; Sammler et al.,
2015) overlap at least partly with those of music processing (Zatorre, Chen & Penhune, 2007; see also Frühholz et al., 2014). Both speech prosody and music rely on the perception of pitch, timbre, intensity and rhythmic sound variations.
The aim of the current study was to investigate potential music and prosody impairments in TBI patients and possible links between the two. Amusia has been previously reported in 35 to 69% of patients having undergone a stroke or a rupture of an aneurysm (located on the middle cerebral artery) one week to seven years post-lesion
(Ayotte et al., 2000; Schuppert et al., 2000; Särkämö et al., 2009), but to our knowledge the prevalence of post-
TBI amusia has never been explored. We also compared prosodic performance in amusic versus non-amusic patient groups. Our hypothesis was that patients with impairments in music would also show impairments in prosody perception, and that the linguistic and emotional dimensions of prosody would be associated with each other. As attentional fatigue is a frequent and long-lasting symptom after a TBI (Belmont, Agar & Azouvi,
2009), we selected two music tests respectively evaluating pitch and rhythm perception, two linguistic prosody tests (one with sentences, the other with a vowel) and two emotional prosody tests (one using sentences, the other using a vowel), and the session did not exceed one hour.
Material and method
Participants
Patients
4 Music and prosody after traumatic brain injury
Several care structures in and around Lyon, France, were contacted to recruit the patients. The majority of the patients were associated with the APF Center in Saint-Martin-en-Haut or the Henry Gabrielle Hospital. The following inclusion criteria were communicated to medical doctors and language therapists in these institutions: patients between 18 and 60 years old, with French as a native language, having undergone a severe traumatic brain injury (Glasgow score ≤9), no longer in the acute phase. We did not recruit participants over 60 years old because TBIs are likely to interact with aging processes, for instance increasing the rate of neurodegenerative diseases (Masel & DeWitt, 2010). Patients also needed to be able to complete our testing session with sufficient motor, behavioral, sensory and attentional abilities. In particular, patients with disorders of consciousness, mutism or hearing disorders were not included. Recruitment was open between October 2018 and February 2019 and thirty-six patients were selected to participate. The study was conducted according to the declaration of
Helsinki. Each participant received an information notice about the study and gave consent. Two pre-tests administered at the beginning of the testing session were used to exclude patients with insufficient short-term memory (forward digit span <5) or insufficient oral understanding (MT-86, Protocole Montréal-Toulouse, oral sentence understanding task with a score <35/38, Nespoulous et al., 1992; see Procedure section). Success on these pre-tests also attested that patients would be able to listen to a series of auditory-verbal stimuli and follow simple instructions. Three patients did not reach a digit span of five items, and one had an insufficient score on the oral understanding task (34/38). One patient lacked sufficient alertness to follow the protocol. Our analyses were thus carried out on data from 31 patients, except for the Lin Vowel task (see below) where data were not acquired for two patients (n=29) for technical reasons. Demographic information is given in Table 1. Only one patient lived independently with his spouse; the majority lived in a medical-care home, or at their parents’ home.
Four patients declared having at least three years of formal piano training (5 years for one patient; 10 years or more for three patients), but all stopped playing after their TBI. When asked about auditory complaints, four patients reported having an auditory hypersensitivity and/or hyperacusis since their brain injury. No patient reported an auditory deficit. One patient had undergone two brain injuries, one 26 years before the protocol, and the other 10 years before. The framework of the study did not allow us to access any additional medical data.
[INSERT TABLE 1 HERE]
Healthy participants for the vowel prosody tests
5 Music and prosody after traumatic brain injury
As the vowel prosody tests were not taken from standardized batteries, we tested 33 healthy participants matched to the patients for age, gender and education. The participants were native French speakers and did not have any neurological or psychiatric history, hearing disorders or musical training. The participants were recruited within the experimenter’s (LLS) circle of friends and among staff members of a hospital cafeteria, targeting the sociodemographic profiles of the patients. A screening for congenital amusia was carried out using the Scale subtest of the Montreal Battery for Evaluation of Amusia (Peretz et al., 2003). Two control participants had a pathological performance on this test (21/30 and 22/30) and were excluded. Standards for the vowel prosody tests were thus established on data from 31 control participants. Demographic information is presented in Table
1.
Material
Music perception
The Scale and Rhythm subtests from the Montreal Battery of Evaluation of Amusia (MBEA, Peretz et al., 2003) were used to assess pitch and rhythm perception. The Scale subtest was selected for its sensitivity; it is considered the best screening test among the six subtests of the MBEA international and standardized battery for music perception disorders (Peretz et al., 2008). In the Scale subtest, participants listen to pairs of short musical sequences and are instructed to judge whether they are identical or different. In the “different” pairs, one note from the second melody is out of tune. The Rhythm subtest is constructed in the same way, except that the
“different” pairs include a rhythmic change. Each subtest comprises 30 trials. We used the original cut-offs to determine a pathological performance: a score below 22/30 for Scale and below 23/30 for Rhythm. These cut- offs correspond to two standard deviations (SD) below the mean of non-amusics’ scores (Peretz et al., 2003).
The Scale and the Rhythm subtests were found to correlate highly with the other subtests of the MBEA in a sample of 44 stroke patients (Särkämö et al., 2009), which suggests that they reasonably reflect overall music perception ability.
Prosody perception
Participants performed the “Emotional Prosody understanding” and “Linguistic Prosody understanding” subtests from the Montreal Evaluation of Communication (MEC, Joanette, Ska, & Côté, 2004). They listened to 24 recorded sentences with neutral content, 12 for emotional prosody and 12 for linguistic prosody. For each
6 Music and prosody after traumatic brain injury sentence, they indicated the emotion (joy, anger, sadness) or the intonation modality (statement, question, order) with a forced-choice answer. Their performance was compared to norms from the original test battery for patients over 30 years old and to Vignaud (2007) for patients under 30. These tests were chosen because they are used in clinical practice for brain-lesioned patient evaluation. However, we anticipated that these tests would lack sensitivity because the pathology cut-off was very low for individuals with less than 11 years of schooling.
We thus ran two other prosody tasks using vowels instead of sentences. The objectives of these two tests were (i) to improve the sensitivity of our testing (ii) to remove the lexico-syntactic dimension patients have to inhibit in sentences to assess the prosodic dimension. Using vowels enabled us to pare down the task to focus only on prosody. Indeed, the semantic dimension is difficult to completely ignore when processing prosody (Besson,
Magne & Schön, 2002; Wambacq & Jerger, 2004). Furthermore, verbal complexity may have a major influence on prosody processing (Mitchell & Ross, 2008), with more bilateral activity corresponding to more complex verbal material to process.
The first test, called Emo Vowel below, was a task of emotion recognition also used in Pralus et al. (2019) based on auditory stimuli created by Charpentier et al. (Charpentier, Kovarski, Roux et al., 2018; Charpentier,
Kovarski, Houy-Durand et al., 2018). Participants listened to recordings of 20 /a/ vowels, four per emotion (see
Figure 1 below, as well as Tables 1a et 1b in Appendix), uttered by eleven different female voices (subset selected from a larger emotional vocalization set, uttered by 15 female actors). The participants then indicated the corresponding emotion (joy, anger, sadness, fear or neutral condition) with a forced-choice answer. After they categorized the emotion of the vowel, they were asked to rate the intensity of the emotion on a 5-point scale
(Pralus et al., 2019), except if their answer was the neutral condition.
A second task, Lin Vowel, was created to assess linguistic prosody perception. Nine /a/ vowels were recorded by two different female voices (respectively four and five vowels) with LogicPro X (version 10.4.6). Loudness was normalized, but fundamental frequencies and spontaneous durations were not modified (see Figure 1).
Participants listened to 12 vowels, the nine recordings, and 3 vowels presented a second time, for a total of four vowels per intonation modality: order, question, neutral. Participants had to indicate the intonation modality with a forced-choice answer. This task was pre-tested with seven adults without neurological history. Following these pilot results, the wording of one of the labels was changed to reduce confusion. The final labels were thus
“Ordre” (order), “Question” (question) and “Intonation neutre” (neutral intonation).
7 Music and prosody after traumatic brain injury
As the two vowel tasks had no referenced norms, the performance of the patients was compared to the performance of our control group.
[INSERT FIG 1 HERE]
Questionnaire
Patients answered a series of demographic and clinical questions, including about their musical experience. Their attitudes to music were explored by questions on how frequently they listened to music and their degree of agreement with the following statements: “Certain kinds of music can put me in a good mood or ‘match’ my current mood”, “Music can help me relax and get rest in certain stressful periods” (inspired by the questionnaire by McDonald & Stewart, 2008). Agreement with each of these statements was indicated on a 4-point Likert scale
(Strongly Disagree, Disagree, Agree, Strongly Agree). The question on the frequency of music listening was open-ended.
Procedure
Patients
Patients were tested individually in a quiet room. Stimuli for computer-based tasks were delivered through open- back headphones. Before the first test, the volume level was adjusted individually to a level that was comfortable for the participant. Testing started with the questionnaire, administered by the experimenter (LLS), and the two inclusion tasks (digit span and oral sentence understanding). The digit span task was stopped when the span of 5 items was validated to prevent patients from becoming fatigued. Oral sentence understanding was tested using the MT-86 test, a sentence-picture matching task (n=38 items; cut-off=35) evaluating syntactic understanding.
The Scale and Rhythm subtests of the MBEA were then administered; patients gave an oral response or pointed to the written forced-choice answers if oral production was difficult. Emo Vowel was then administered with a written document containing the instructions and forced-choice answers. This task had two instructions: to categorize an emotion and evaluate its intensity. Patients then performed the linguistic and emotional prosody understanding subtests of the MEC battery, and finally, the Lin Vowel test, with a visual document illustrating the forced-choice answers. Breaks were offered if needed. Each test generated an individual score representing the percentage of correct answers.
8 Music and prosody after traumatic brain injury
Healthy participants for the vowel prosody tests
The control participants took the MBEA Scale subtest in order to check for the absence of congenital amusia.
They then performed the Emo Vowel and Lin Vowel tests. MBEA Rhythm and MEC battery tests were not performed, as we used the published norms to evaluate patients’ performances. Only the demographic questions of the questionnaire were administered. The length of the testing session was 20 minutes.
Data analysis
We ran individual analyses to report the number of patients with a pathological score in each of the tasks, and group comparisons for the vowel prosody tests performed by both our patients and controls. We considered a score as pathological when equal to or below the cut-off indicated in the original battery norms (MBEA, MEC) or when equal to or below two SDs from the mean of our control group for the vowel prosody tasks. We also divided the patients into an amusic and a non-amusic group. We used the average of the Scale and Rhythm scores as a marker of amusia (as done for instance by Särkämö et al., 2009, in their study on music perception in stroke patients). The cut-off score was 75% of correct answers (22.5 points out of 30), following the cut-off for the average of the Scale and Rhythm scores in the original MBEA (Peretz et al., 2003; and similar to Särkämö et al., 2009). Scale and Rhythm scores were significantly correlated with each other across our patients (r=.44, p=.007). Prosody understanding was compared between the amusic and non-amusic groups.
Normality of data was violated for the patients’ scores on the MEC tasks (Emotional: W=.842, p<.001;
Linguistic: W=.881, p=.003). Mann-Whitney U tests were thus used to compare amusic and non-amusic patients.
Finally, relationships between the tests were evaluated using Spearman correlations.
Results
Amusia
At the individual level, 42% of the patients in our sample had a pathological score on the Scale test, i.e., in detecting an out-of-key note in a pair of melodies, and 52% of the patients had a pathological score on the
Rhythm test, i.e., in discriminating a rhythmic change in a pair of melodies. The amusic group (mean score on the Scale and Rhythm subtests <75%) was composed of 13 patients and the non-amusic group (mean score
9 Music and prosody after traumatic brain injury
≥75%) of 18 patients (n=16 for Lin Vowel). There were no significant differences between the amusic and non- amusic groups when they were compared for age, musical background (years of instrument playing), education and gender (n=5 women in each group; see Table 3). Time post-injury was marginally higher in the amusic group (p=.065).
Deficits in understanding prosody
Performance in the four prosody tests was significantly above chance in our patient group. (Emo Vowel: chance
=20% of correct responses; mean score=56%; one-tailed one-sample t-test t(30)=10.385, p<.001; Cohen’s d=1.865. Lin Vowel: chance=33% of correct responses; mean score=69%±0.23; one-tailed one-sample t-test t(28)=8.388, p<.001, Cohen’s d=1.558. MEC-Emo: chance=33% of correct responses; median score=83%;
Wilcoxon signed-rank test: V=496, p<.001, rank-biserial correlation (effect size): 1.000. MEC-Lin: chance=33% of correct responses; median score=83%; Wilcoxon signed-rank test: V=.456, p<.001, rank-biserial correlation
(effect size): 0.839.)
In comparison to the cut-off, 71% of our patients (22/31) showed impairment in at least one of the four prosody scores (emotional or linguistic prosody understanding in sentences or vowels), as illustrated in Table 2. Thirty- two percent of the patients demonstrated both linguistic and emotional prosody impairment (in sentences and/or vowels). There were similar frequencies of patients with linguistic or emotional impairment (48% of patients on the emotional test and 55% of patients on the linguistic test were below the cut-off, i.e -2SDs below the mean of the controls).
The Vowel tasks were more sensitive than the prosody understanding tests with sentences from the MEC. In the
Vowel tasks on emotional prosody, 55% of patients obtained a pathological score versus 6% for the MEC sentences. For linguistic prosody, 55% of patients had a pathological score for the vowels versus 13% for the
MEC sentences.
At the group level, emotional prosody perception for vowels (the Emo Vowel task) was significantly poorer in patients than in controls (U=820, p<.001, Cohen’s d=1.11), as illustrated in Figure 2. In contrast, emotion intensity ratings were not significantly different between the two groups (Patient mean: 2.98±0.74; Control mean: 2.81±0.53 on a 5-point scale; Welch t-test: t(54.203)=-1.016, p=.314). However, items categorized with the wrong emotion were excluded from this analysis. As 15 patients had more than 50% of wrongly categorized items, the total number of items included in each individual average was low for patients, and this result should be interpreted with caution.
10 Music and prosody after traumatic brain injury
[INSERT FIG 2 HERE]
Linguistic prosody perception in vowels (Lin Vowel) was also significantly poorer in patients than in controls
(U=826, p<.001, Cohen’s d=1.11; see Figure 2). Results for each emotional and linguistic category are provided in the Appendices.
Within the patient group, females’ performance (n=10) was not significantly different from males’ performance
(n=21) across the four prosody tasks: U>69, p>.332.
[INSERT TABLE 2 HERE]
Links between tasks
The amusic patients performed worse than non-amusic patients on the four prosody tests (ps<.023, see Table 3).
[INSERT TABLE 3 HERE]
As illustrated in Table 4, performances in all the music and prosody tasks were significantly correlated, with moderate or strong links. Tests of correlation comparisons from dependent samples revealed that emotional prosody scores (sentences and vowels) were marginally more correlated to the Rhythm than to the Scale score
(MEC-emo: z=-1.477, p=.070; Emo Vowel: z=-1.444, p=.074; single sided testing). Correlations of linguistic prosody scores with Rhythm and with Scale were not significantly different (z≤0.755, p≥.225 for sentences and vowels).
[INSERT TABLE 4 HERE]
Attitude to music
Seventy-seven percent of the patients (n=24) agreed with the statement “Music may help in stressful periods” and 74% (n=23) with “Certain kinds of music can put me in a good mood” (“Agree” or “Strongly Agree” answers); several spontaneously reported that music helped them manage their handicap. Among the patients who did not agree with one or both statements, only two were amusic, suggesting that amusia was not the cause of poor emotional experience. Twenty-two percent of the patients (n=7) reported listening to music only
11 Music and prosody after traumatic brain injury
“sometimes,” “rarely” or significantly less than before the TBI. Among the seven patients, five did not agree with the statements about the emotional power of music; two were amusic.
Discussion
Results of the present study in a sample of patients with severe TBI (n=31) with mixed times post-onset indicate
(i) frequent amusia (42% of our patient sample), (ii) frequent impairments in emotional and linguistic prosody decoding (respectively 42% of the patients and 55% of the patients) and (iii) more prosody deficits in amusic patients compared to non-amusic patients.
Amusia
This is, to our knowledge, the first study showing an alteration of melodic perception in TBI patients. Drapeau et al. (2017) did not find any deficits in TBI individuals’ discrimination of musical sequences. Balzani et al. (2014) found a deficit only in the rhythmic dimension. However, the average severity of the TBI was lower in both studies. Our data reveals that amusia, as determined by impaired performance on the MBEA (Scale and Rhythm subtests), is a common and long-lasting deficit following a severe TBI. The prevalence of amusia we observed is similar to the estimated prevalence in patients having undergone a stroke or rupture of an aneurysm on the middle cerebral artery: respectively 35 and 42% of patients three months to seven years post-lesion were affected in the studies by Ayotte et al. (2000) and Särkämö et al. (2009)1.
The majority of our patients reported a positive relationship to music (around three out of four agreed with the fact that music benefits their mood and stress regulation). Nonetheless, this rate of agreement is low compared to other data reporting 100% of agreement in an adult population of non-musicians (McDonalds and Stewart,
2008). In a study on 78 brain-damaged patients (mainly due to strokes) conducted by Belfi et al. (2017), 9% of patients had general anhedonia and 6% had music-specific anhedonia, preventing them from enjoying music.
Preliminary data from Balzani et al. (2014) also revealed that a majority of (mild) TBI patients reported a decrease in music listening and less enjoyment. The present study confirms that a reduced emotional experience when listening to music is sometimes associated with TBI, independently of amusia. Nonetheless, our data does not disentangle the effects of post-TBI environmental changes (the availability of music) from anhedonia, nor does it pinpoint the causes of the poorer emotional experience. Future studies could address the question of anhedonia for music and/or other stimuli in TBI patients using tools such as those developed by Mas-Herrero et
1 Note that Schuppert et al.(2000) found a higher prevalence (69% of amusias among their stroke patients sample) because the tests were performed only 5-10 days post-lesion. 12 Music and prosody after traumatic brain injury al. (2014) targeting subjective and objective and/or conscious and unconscious emotional responses. The presence of depression and general anhedonia (non-specific to music) will also have to be assessed to diagnose musical anhedonia.
Impairments in prosody decoding
Half of our sample presented a deficit in prosody. The prevalence of the deficit was similar to that found in a population of stroke patients: affective prosody was altered in 48% of patients with a right hemisphere stroke in a study by Wright et al. (2016) and over half in a study by Sheppard et al. (2020). The linguistic and emotional dimensions of prosody were both frequently affected in our patient group when tested with a sensitive task. A comparison of our control and patient groups in linguistic and emotional prosody yielded the same group effect sizes. A deficit in emotion perception following a TBI has been frequently described in the literature (see Ilie et al., 2017, for a review of seven studies on labeling emotions in prosody post TBI). However, linguistic prosody perception post TBI has been understudied and has yielded inconsistent results (Milders et al., 2003; Ietswaart et al., 2008). Prosody impairments in TBI patients may be due not (only) to lesions in areas involved in emotions such as the orbito-frontal cortex, but to lesions in areas that process both linguistic and emotional cues in the voice, such as the superior temporal gyrus (pSTG) and the right dorsolateral frontal cortex (Wildgruber et al.,
2004, Schirmer & Kotz, 2006). Damage to the right pSTG (involved in processing acoustic features like pitch) was found to correlate to poor performance in affective prosody in injured patients (Sheppard et al., 2020), and this area is also involved in processing linguistic prosody (Belyk & Brown, 2014). Alterations to the right superior longitudinal fasciculus, which supports prosody processing (Sammler et al., 2015), are also a likely explanation. This tract, as well as several other major fiber bundles, is durably impaired in TBI patients (Bendlin et al., 2008). The tract appears to be involved in the ability to parse and label a dynamic prosodic contour, as well as coupling perception to motor representations (Sammler et al., 2015; 2018). The ventral pathway may also serve in emotional prosody perception (Schirmer & Kotz, 2006). The right inferior fronto-occipital fasciculus, for instance, has been found to be part of the network involved in emotional prosody decoding (Frühholz et al.,
2015). Finally, the impact of personality on the processing of prosody and its substrates could be explored deeper, as neuroticism, a personality trait which is more frequent in individuals with TBI than in the general population (Rigon et al., 2019), may modulate the activations observed in fMRI during prosody decoding (Brück et al., 2011).
13 Music and prosody after traumatic brain injury
The majority of the previous studies on prosody decoding after TBI used sentences with lexico-syntactic content to evaluate emotional prosody (e.g Dimoska et al.2010; Ietswaart et al., 2008; McDonald & Saunders, 2005;
Milders et al., 2008). However, to perform a categorization task and focus on prosodic features, listeners need to inhibit lexico-syntactic content, which is not relevant to the task but is salient (semantic processing bias, Besson et al., 2002, Wambacq et al., 2004). These inhibition processes may be deficient in brain-lesioned patients (e.g.
Schmitter-Edgecombe & Kibby, 1998), especially when the association between the lexico-syntactic content and the prosodic pattern is artificial and non-ecological. The present study shows prosody impairment using material without lexical and syntactic content (vowels), which also reduces the demands on attention (see also Dimoska et al., 2010). In parallel, it reduces the number of available cues: our patients analyzed emotion using a stimulus lasting less than one second. As expected, the tasks with the vowel material were found to be more sensitive than the tasks with sentences from the MEC. A similar observation was made by Pralus et al. (2019) in congenital amusia.
The results of Rigon et al. (2016) showing a relative preservation of facial affect recognition in females compared to males after TBI were not replicated with our prosodic material.
Links between amusia and prosody impairments
Our third main result is that amusia is associated with prosody impairments. Prosody is essentially processed in a right fronto-temporal network (Schirmer & Kotz, 2006; Belyk & Brown, 2014), with a dorsal and a ventral pathway (Frühholz et al., 2015; Sammler et al., 2015), a network similar to music network. Some studies directly compared song and speech processing and found substantial neural overlap (e.g., Schön et al., 2010; Merrill et al., 2012; for a review and discussion, see Peretz, 2015). However, neuroimaging studies directly comparing prosody perception (and not speech in general) to music perception are scarce. Cases of impairments both in music and prosody perception have been reported (in acquired amusia, e.g Confavreux et al., 1992; Patel et al.,
1998; in congenital amusia, Stewart, 2008; Patel et al., 2008b; Liu et al., 2010; Lolli et al., 2015; Thompson et al., 2012; Pralus et al., 2019). A study by Sihvonen et al. (2019) on stroke patients showed that the right dual- stream network was affected in amusic patients. Furthermore, in this study, the right inferior fronto-occipital fasciculus, which is involved in emotional prosody decoding, was the main predictor of MBEA performance over time (reflecting the degree of recovery from amusia).
14 Music and prosody after traumatic brain injury
Previous studies focusing on emotional prosody post-TBI (Dimoska et al., 2010; Ilie et al., 2017; McDonalds &
Saunders, 2005; Zupan et al., 2014) might be interpreted as evidence of emotional deficits in patients. Our results show that linguistic prosody is equally impaired, suggesting that the processing of acoustic features and/or higher-order cognitive processes are altered (possibly in addition to emotion categorization). These processes are also partially shared by music (Zatorre & Baum, 2012). Pitch dynamic and rhythm, but also loudness dynamic, are central components to process to interpret prosody and music (Juslin & Laukka, 2003). In our results, prosody decoding performance correlated significantly with the Rhythm and the Scale scores. The strongest link was the correlation between the emotional prosody tests and the Rhythm test. Hausen et al. (2013) also found that word stress perception in prosody correlated significantly with the Rhythm test but not with the Scale test in healthy participants, suggesting that rhythmic skills are on the front of the stage in prosody decoding (see also e.g., Magne et al., 2016). At a higher-level, prosody and music decoding both rely on auditory attention and working memory abilities. For instance, attention seems to boost sensory encoding in primary auditory areas
(Alho et al., 2014). The present study did not finely assess the attentional and working memory skills (apart from the tests used as inclusion tests, checking that the short-term memory span and oral understanding were sufficient to perform the tasks) and this study does not allow to conclude on the influence of these higher-order factors on the observed effects. Further research is necessary to explore to what extent the association between post-TBI speech and music impairments is modulated by acoustic processing and other more general cognitive functions.
Diagnosing prosody impairments in a more systematic way and taking them into account in remediation programs could have a significant impact on social and professional reintegration. As shown in a study on healthy young adults, higher prosody decoding skills correlate with psychological and relational well-being
(Carton, Kessler & Pape, 1999). This correlation has also been found in stroke patients with left-hemisphere damage: their performance in prosody decoding was found to correlate with social and emotional subscales in a questionnaire on quality of life (Leung et al., 2017). In a study on stroke patients with right-hemisphere damage, relationship (marital) satisfaction was correlated with nonaffective prosody discrimination (Blonder et al., 2012).
Injured individuals exhibit higher levels of depression and anxiety (Ilie et al., 2017), and this may be linked in part to poor social skills and communicative deficits. Music could be a privileged medium to improve prosodic skills (Thompson et al., 2003; 2004), in addition to its effects on mood and social interactions already observed in injured patients (Nayak et al., 2000). Remediation could also include training in acoustic processing.
15 Music and prosody after traumatic brain injury
Limitations
The collected data does not enable us to distinguish between congenital amusia and acquired amusia. Only the abnormally high number of cases in our sample and qualitative comments from the patients suggested that their impairments were probably acquired and not congenital. For instance, 42% of our patients obtained a pathological score on the Scale Test, while congenital amusia has a prevalence of 1.5% in the general population according to Peretz & Vuvan (2017). Qualitative comments included answers to the question “Music may help in stressful periods” such as “Yes, before; but now music has no effect” and reports of a drop in the frequency of music listening. However, three of our patients self-reported poor musical skills before the injury. Another limitation to our study was our choice to not use the entire MBEA battery for the diagnosis of amusia to avoid patient fatigue. However, the Scale subtest is considered the most discriminant subtest from this battery (Peretz et al., 2008). Other studies have also used this subtest in association with a rhythm test to diagnose amusia when using the entire MBEA was not possible (e.g. Särkämö et al., 2009; Hausen et al., 2013).
The present study does not elucidate the nature of the links between music and prosody impairments. The high prevalence of amusia and prosody deficits in our sample may evoke more general disorders of attention and working memory which could have contributed to our patients’ pathological scores. Even if attention and working memory impairments are indeed common following a TBI, all of our patients were nonetheless able to succeed in at least one of the music or prosody tasks, showing that their attention and working memory were sufficient, as expected following our two pre-tests. In the future, research in music and prosody perception needs to further explore the interplay between acoustic processing skills and higher-level cognitive functions.
Finally, our data does not allow us to correlate the performance to indicators of trauma severity. The lack of lesional and more globally clinical data about the patients is an important limitation of this study.
Conclusion
Our study indicates that severe TBI is frequently associated with impairments in music perception and prosody decoding. These deficits are reported for patients several months or years after their trauma and with sufficient short-term memory and linguistic abilities to perform the tests. The emotional and linguistic dimensions of prosody were equally altered for the patients. Amusic patients showed more prosody deficits than non-amusic patients. While future work is needed to further investigate the causal factors underlying these symptoms and pinpoint the level or depth of the dysfunction, our study proves that difficulties in music and prosody perception are not anecdotal. When diagnosing a deficit in emotional prosody perception, pitch perception could be
16 Music and prosody after traumatic brain injury explored with a fine-grained investigation, and rehabilitation programs targeting melody and rhythm perception could be developed. By improving interpersonal communication skills, this line of work could result in better functional outcomes at the individual and societal levels for injured individuals.
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28 Music and prosody after traumatic brain injury
Appendices
Table 1a: Acoustic parameters for Lin Vowel stimuli, averaged across the exemplars of a given linguistic category, with the standard error of the mean within brackets. Stimuli were equalized in Root Mean Square
(RMS) amplitude.
Order Question Neutral Duration (ms) 329(7) 362(35) 693(61) SD intensity 12(0) 10(2) 7(1) f0 (Hz) 268(2) 306(21) 231(9) SD f0 19(3) 119(5) 4(0)
Table 1b: Acoustic parameters for Emo Vowel stimuli, averaged across the exemplars of a given emotional category, with the standard error of the mean within brackets. Stimuli were equalized in Root Mean Square
(RMS) amplitude and lasted 400ms. Other parameters for these stimuli are presented in Pralus et al. (2019).
Joy Neutral Fear Sadness Anger SD intensity 8(2) 0(0) 6(2) 1(0) 4(1) f0 (Hz) 300(30) 224(9) 406(22) 227(1) 252(16) SD f0 40(8) 1(0) 26(5) 9(2) 33(5)
29 Music and prosody after traumatic brain injury
Results by condition and modality for Emo Vowel and Lin Vowel
In the patient group, as illustrated in Table 1a, joy was the most recognized emotion in Emo vowel and sadness was the least recognized, with a high level of confusion with the neutral condition. The pattern was similar in the control group with higher performances. Note that there were not equal proportions of positive and negative emotions in these tasks, and negative emotions were confused more often.
Table 2a: Patients’ results for Emo vowel
Expected/Given Fear Neutral Anger Joy Sadness Fear 52,42% 16,13% 5,65% 21,77% 4,03% Neutral 15,32% 58,87% 9,68% 9,68% 6,45% Anger 18,55% 16,13% 40,32% 17,74% 7,26% Joy 2,42% 7,26% 3,23% 80,65% 6,45% Sadness 14,52% 39,52% 4,84% 11,29% 29,84%
Table 2b: Controls’ results for Emo vowel
Expected/Given Fear Neutral Anger Joy Sadness Fear 75,00% 5,65% 7,26% 7,26% 4,84% Neutral 3,23% 72,58% 2,42% 12,90% 8,87% Anger 9,68% 7,26% 61,29% 15,32% 6,45% Joy 0,81% 4,03% 1,61% 91,13% 2,42% Sadness 5,65% 29,03% 0,81% 8,06% 56,45%
In Lin Vowel, as illustrated in Table 2a, ‘question’ was the best recognized modality for the patient group, and
‘neutral’ modality was the least recognized. The pattern was similar in the control group with higher performances.
Table 3a: Patients’ results for Lin Vowel
Questio Expected/Given n Neutral Order Question 78,33% 13,79% 7,88% Neutral 20,11% 63,79% 16,09% Order 12,81% 20,20% 67,00%
Table 3b: Controls’ results for Lin Vowel
30 Music and prosody after traumatic brain injury
Questio Expected/Given n Neutral Order Question 98,21% 1,34% 0,45% Neutral 13,02% 83,85% 3,13% Order 2,23% 4,46% 93,30%
31 Music and prosody after traumatic brain injury
Funding: This work was carried out within the framework of the LABEX CeLyA (ANR-10-LABX-0060) of the University of Lyon.
Conflicts of interest/Competing interests: On behalf of both authors, the corresponding author states that there is no conflict of interest.
Acknowledgement: We thank Annie Chalivet, Valérie Morel, Pr. Jacques Luauté, Emmanuelle Aujogues,
Monique Sanchez and Emmanuelle Jean for their precious help in recruiting patients, opening the doors of their care home or hospital unit. We also thank Nicolas Léard for help in programming and data analyses, Anne
Caclin for advice in prosody assessment, and Barbara Tillmann, Anne Caclin and Oriana Reid-Collins for their feedback on the manuscript.
Corresponding author: [email protected]
95 Bd Pinel – Hospital Le Vinatier – Lyon Neuroscience Research Centre (CRNL) – Neurocampus
69500 BRON, FRANCE
32 Music and prosody after traumatic brain injury
Controls for the vowel Statistics and p-value Patients (n=31) prosody tests (n=31) W=453, p=0.704 Age (years) 38.10 (12.14) 37.29 (13.57)
Gender (% women) 32% 32% W=485.5, p=0.948 Schooling (years) 11.61 (3.08) 11.68 (2.33)
Musical training (years) 0.74 (2.32) 0
Time post-TBI -
Less than 2 years 25% -
Between 2 and 5 years 23% -
Between 5 and 10 years 52% -
Table 1: Sociodemographic data of patients and control participants included in the analyses (after exclusions detailed in Section 2.1). SDs are indicated between brackets. A Wilcoxon test was chosen to compare groups because the distribution of the data was not normal.
33 Music and prosody after traumatic brain injury
Patient Sex Age Scale Rhythm Emo Vowel Lin Vowel MEC Lin MEC Emo 1 M 38 93% 67% 50% 70% 83% 75% 2 M 38 73% 83% 50% 45% 25% 42% 3 M 55 63% 40% 35% 40% 42% 58% 4 F 31 83% 83% 90% 83% 92% 5 M 35 50% 73% 40% 75% 58% 100% 6 F 52 57% 63% 35% 40% 50% 75% 7 F 29 63% 70% 70% 55% 92% 92% 8 M 47 53% 50% 40% 30% 8% 50% 9 F 27 73% 67% 40% 60% 75% 67% 10 M 35 67% 60% 60% 60% 67% 83% 11 M 55 60% 67% 30% 20% 33% 75% 12 M 25 80% 83% 30% 85% 58% 92% 13 M 33 93% 87% 60% 70% 100% 100% 14 M 29 77% 53% 40% 70% 67% 50% 15 M 25 87% 70% 80% 100% 92% 75% 16 F 25 73% 83% 65% 70% 83% 100% 17 F 49 93% 80% 60% 80% 83% 100% 18 M 30 70% 87% 50% 85% 92% 83% 19 F 49 70% 87% 60% 65% 92% 83% 20 F 25 77% 60% 40% 80% 83% 100% 21 M 57 83% 73% 55% 30% 42% 42% 22 M 23 70% 77% 60% 55% 75% 83% 23 F 59 50% 50% 25% 55% 58% 58% 24 M 47 77% 60% 35% 100% 92% 58% 25 M 19 87% 70% 50% 95% 100% 100% 26 M 23 77% 77% 90% 95% 100% 100% 27 M 57 90% 90% 90% 100% 83% 100% 28 M 40 70% 90% 85% 95% 83% 100% 29 M 43 80% 93% 70% 90% 92% 100% 30 F 33 77% 77% 75% 75% 100% 100% 31 M 48 97% 90% 70% 100% 100%
Table 2: Percentage of correct answers on the music and prosody tests for each patient. The grey color indicates a pathological score (-2SDs from the reference score). The reference scores are the norms published for the MBEA (Scale and Rhythm) tests and the MEC tests, and the means and SD of our control group for the Vowel tests. Note that the MEC tests have different cut-offs depending on age and education.
34 Music and prosody after traumatic brain injury
W p Rank-Biserial Correlation Age 130 0.616 0.111 Education (years) 114 0.919 -0.026 Musical training 130. 0.498 0.115 (years) 5 Time post-injury 163. 0.065 0.397 (years) 5 Emo Vowel 34.5 < .001* -0.705 Lin Vowel 46 0.011* -0.558 MEC-Lin 49.5 0.007* -0.577 MEC-Emo 61 0.022* -0.479
Table 3: Comparison of amusic and non-amusic patients with Mann-Whitney U tests. Rank-biserial correlation indicates the effect size. A star indicates a significant difference between groups.
35 Music and prosody after traumatic brain injury
Table 4: Positive correlations between the 6 music and prosody tasks in patients (df = 29). Applying a Bonferroni correction for multiple correlations lowers the significance threshold of each test to 0.0033.
36 Music and prosody after traumatic brain injury
Figure captions
Fig. 1: Examples of stimuli used in Lin Vowel and Emo Vowel. The spectrogram, waveform and pitch contour of one representative stimulus by category are represented.
Fig. 2: Average results of both groups on emotion recognition in vowel tasks. Error bars correspond to standard error.
37 Music and prosody after traumatic brain injury
Figure 1
38 Music and prosody after traumatic brain injury
100% 90% 80% 70% 60% e
r 50% o c S 40% 30% 20% 10% 0% Emo Vowel Lin Vowel
Patients Controls
Figure 2
39