The genetics of congenital amusia (tone deafness): a family-aggregation study

Congenital amusia (commonly known as “tone deafness”) is a lifelong impairment of music perception that affects 4% of the population. To estimate whether congenital amusia can be genetically transmitted, its prevalence was quantified by direct auditory testing of 71 members of 9 large families of amusic probands, as well as of 75 members of 10 control families. The results confirm that congenital amusia is expressed by a deficit in processing musical pitch but not musical time and also show that the pitch disorder has a hereditary component. In amusic families, 39% of first-degree relatives have the same cognitive disorder, whereas only 3% have it in the control families. The identification of multiplex families with a high relative risk of experiencing a musical pitch deficit (λ_s=10.8; 95% confidence interval 8–13.5) enables the mapping of genetic loci for hereditary amusia.     

先天性音乐障碍者音乐加工障碍及其特异性争议

人群中存在少量先天性音乐障碍(congenital amusia)个体,表现出音乐感知和表达方面有选择性障碍。本文总结了前人甄别先天性音乐障碍个体的工具,述评了先天性音乐障碍者对音乐加工时的障碍表现,以及先天性音乐障碍者其障碍领域特异性争议,并从行为遗传学和音乐加工脑机制角度,综述了先天性音乐障碍者可能的原因,最后对先天性音乐障碍未来可能的研究方向做了四个方面的展望。     

Congenital amusia: a disorder of fine-grained pitch discrimination.

We report the first documented case of congenital amusia. This disorder refers to a musical disability that cannot be explained by prior brain lesion, hearing loss, cognitive deficits, socioaffective disturbance, or lack of environmental stimulation. This musical impairment is diagnosed in a middle-aged woman, hereafter referred to as Monica, who lacks most basic musical abilities, including melodic discrimination and recognition, despite normal audiometry and above-average intellectual, memory, and language skills. The results of psychophysical tests show that Monica has severe difficulties with detecting pitch changes. The data suggest that music-processing difficulties may result from problems in fine-grained discrimination of pitch, much in the same way as many language-processing difficulties arise from deficiencies in auditory temporal resolution.     

The Amusic Brain: Lost in Music,but Not in Space

Congenital amusia is a neurogenetic disorder of music processing that is currently ascribed to a deficit in pitch processing. A recent study challenges this view and claims the disorder might arise as a consequence of a general spatial-processing deficit. Here, we assessed spatial processing abilities in two independent samples of individuals with congenital amusia by using line bisection tasks (Experiment 1) and a mental rotation task (Experiment 2). Both amusics and controls showed the classical spatial effects on bisection performance and on mental rotation performance, and amusics and controls did not differ from each other. These results indicate that the neurocognitive impairment of congenital amusia does not affect the processing of space.     

Amusia Results in Abnormal Brain Activity following Inappropriate Intonation during Speech Comprehension

Pitch processing is a critical ability on which humans' tonal musical experience depends, and which is also of paramount importance for decoding prosody in speech. Congenital amusia refers to deficits in the ability to properly process musical pitch, and recent evidence has suggested that this musical pitch disorder may impact upon the processing of speech sounds. Here we present the first electrophysiological evidence demonstrating that individuals with amusia who speak Mandarin Chinese are impaired in classifying prosody as appropriate or inappropriate during a speech comprehension task. When presented with inappropriate prosody stimuli, control participants elicited a larger P600 and smaller N100 relative to the appropriate condition. In contrast, amusics did not show significant differences between the appropriate and inappropriate conditions in either the N100 or the P600 component. This provides further evidence that the pitch perception deficits associated with amusia may also affect intonation processing during speech comprehension in those who speak a tonal language such as Mandarin, and suggests music and language share some cognitive and neural resources.     

Effects of culture on musical pitch perception

The strong association between music and speech has been supported by recent research focusing on musicians' superior abilities in second language learning and neural encoding of foreign speech sounds. However, evidence for a double association--the influence of linguistic background on music pitch processing and disorders--remains elusive. Because languages differ in their usage of elements (e.g., pitch) that are also essential for music, a unique opportunity for examining such language-to-music associations comes from a cross-cultural (linguistic) comparison of congenital amusia, a neurogenetic disorder affecting the music (pitch and rhythm) processing of about 5% of the Western population. In the present study, two populations (Hong Kong and Canada) were compared. One spoke a tone language in which differences in voice pitch correspond to differences in word meaning (in Hong Kong Cantonese, /si/ means 'teacher' and 'to try' when spoken in a high and mid pitch pattern, respectively). Using the On-line Identification Test of Congenital Amusia, we found Cantonese speakers as a group tend to show enhanced pitch perception ability compared to speakers of Canadian French and English (non-tone languages). This enhanced ability occurs in the absence of differences in rhythmic perception and persists even after relevant factors such as musical background and age were controlled. Following a common definition of amusia (5% of the population), we found Hong Kong pitch amusics also show enhanced pitch abilities relative to their Canadian counterparts. These findings not only provide critical evidence for a double association of music and speech, but also argue for the reconceptualization of communicative disorders within a cultural framework. Along with recent studies documenting cultural differences in visual perception, our auditory evidence challenges the common assumption of universality of basic mental processes and speaks to the domain generality of culture-to-perception influences.     

The mechanism of speech processing in congenital amusia: evidence from Mandarin speakers

Congenital amusia is a neuro-developmental disorder of pitch perception that causes severe problems with music processing but only subtle difficulties in speech processing. This study investigated speech processing in a group of Mandarin speakers with congenital amusia. Thirteen Mandarin amusics and thirteen matched controls participated in a set of tone and intonation perception tasks and two pitch threshold tasks. Compared with controls, amusics showed impaired performance on word discrimination in natural speech and their gliding tone analogs. They also performed worse than controls on discriminating gliding tone sequences derived from statements and questions, and showed elevated thresholds for pitch change detection and pitch direction discrimination. However, they performed as well as controls on word identification, and on statement-question identification and discrimination in natural speech. Overall, tasks that involved multiple acoustic cues to communicative meaning were not impacted by amusia. Only when the tasks relied mainly on pitch sensitivity did amusics show impaired performance compared to controls. These findings help explain why amusia only affects speech processing in subtle ways. Further studies on a larger sample of Mandarin amusics and on amusics of other language backgrounds are needed to consolidate these results.     

Music perception: sounds lost in space

A recent study of spatial processing in amusia makes a controversial claim that such musical deficits may be understood in terms of a problem in the representation of space. If such a link is demonstrated to be causal, it would challenge the prevailing view that deficits in amusia are specific to the musical or even the auditory domain.     

Auditory and cognitive deficits associated with acquired amusia after stroke: a magnetoencephalography and neuropsychological follow-up study

Acquired amusia is a common disorder after damage to the middle cerebral artery (MCA) territory. However, its neurocognitive mechanisms, especially the relative contribution of perceptual and cognitive factors, are still unclear. We studied cognitive and auditory processing in the amusic brain by performing neuropsychological testing as well as magnetoencephalography (MEG) measurements of frequency and duration discrimination using magnetic mismatch negativity (MMNm) recordings. Fifty-three patients with a left (n = 24) or right (n = 29) hemisphere MCA stroke (MRI verified) were investigated 1 week, 3 months, and 6 months after the stroke. Amusia was evaluated using the Montreal Battery of Evaluation of Amusia (MBEA). We found that amusia caused by right hemisphere damage (RHD), especially to temporal and frontal areas, was more severe than amusia caused by left hemisphere damage (LHD). Furthermore, the severity of amusia was found to correlate with weaker frequency MMNm responses only in amusic RHD patients. Additionally, within the RHD subgroup, the amusic patients who had damage to the auditory cortex (AC) showed worse recovery on the MBEA as well as weaker MMNm responses throughout the 6-month follow-up than the non-amusic patients or the amusic patients without AC damage. Furthermore, the amusic patients both with and without AC damage performed worse than the non-amusic patients on tests of working memory, attention, and cognitive flexibility. These findings suggest domain-general cognitive deficits to be the primary mechanism underlying amusia without AC damage whereas amusia with AC damage is associated with both auditory and cognitive deficits.     

Electromagnetic correlates of musical expertise in processing of tone patterns

Using magnetoencephalography (MEG), we investigated the influence of long term musical training on the processing of partly imagined tone patterns (imagery condition) compared to the same perceived patterns (perceptual condition). The magnetic counterpart of the mismatch negativity (MMNm) was recorded and compared between musicians and non-musicians in order to assess the effect of musical training on the detection of deviants to tone patterns. The results indicated a clear MMNm in the perceptual condition as well as in a simple pitch oddball (control) condition in both groups. However, there was no significant mismatch response in either group in the imagery condition despite above chance behavioral performance in the task of detecting deviant tones. The latency and the laterality of the MMNm in the perceptual condition differed significantly between groups, with an earlier MMNm in musicians, especially in the left hemisphere. In contrast the MMNm amplitudes did not differ significantly between groups. The behavioral results revealed a clear effect of long-term musical training in both experimental conditions. The obtained results represent new evidence that the processing of tone patterns is faster and more strongly lateralized in musically trained subjects, which is consistent with other findings in different paradigms of enhanced auditory neural system functioning due to long-term musical training.     

Cortical plasticity induced by short-term multimodal musical rhythm training

Performing music is a multimodal experience involving the visual, auditory, and somatosensory modalities as well as the motor system. Therefore, musical training is an excellent model to study multimodal brain plasticity. Indeed, we have previously shown that short-term piano practice increase the magnetoencephalographic (MEG) response to melodic material in novice players. Here we investigate the impact of piano training using a rhythmic-focused exercise on responses to rhythmic musical material. Musical training with non musicians was conducted over a period of two weeks. One group (sensorimotor-auditory, SA) learned to play a piano sequence with a distinct musical rhythm, another group (auditory, A) listened to, and evaluated the rhythmic accuracy of the performances of the SA-group. Training-induced cortical plasticity was evaluated using MEG, comparing the mismatch negativity (MMN) in response to occasional rhythmic deviants in a repeating rhythm pattern before and after training. The SA-group showed a significantly greater enlargement of MMN and P2 to deviants after training compared to the A- group. The training-induced increase of the rhythm MMN was bilaterally expressed in contrast to our previous finding where the MMN for deviants in the pitch domain showed a larger right than left increase. The results indicate that when auditory experience is strictly controlled during training, involvement of the sensorimotor system and perhaps increased attentional recources that are needed in producing rhythms lead to more robust plastic changes in the auditory cortex compared to when rhythms are simply attended to in the auditory domain in the absence of motor production.     

Experience Changes How Emotion in Music Is Judged: Evidence from Children Listening with Bilateral Cochlear Implants,Bimodal Devices,and Normal Hearing

Children using unilateral cochlear implants abnormally rely on tempo rather than mode cues to distinguish whether a musical piece is happy or sad. This led us to question how this judgment is affected by the type of experience in early auditory development. We hypothesized that judgments of the emotional content of music would vary by the type and duration of access to sound in early life due to deafness, altered perception of musical cues through new ways of using auditory prostheses bilaterally, and formal music training during childhood. Seventy-five participants completed the Montreal Emotion Identification Test. Thirty-three had normal hearing (aged 6.6 to 40.0 years) and 42 children had hearing loss and used bilateral auditory prostheses (31 bilaterally implanted and 11 unilaterally implanted with contralateral hearing aid use). Reaction time and accuracy were measured. Accurate judgment of emotion in music was achieved across ages and musical experience. Musical training accentuated the reliance on mode cues which developed with age in the normal hearing group. Degrading pitch cues through cochlear implant-mediated hearing induced greater reliance on tempo cues, but mode cues grew in salience when at least partial acoustic information was available through some residual hearing in the contralateral ear. Finally, when pitch cues were experimentally distorted to represent cochlear implant hearing, individuals with normal hearing (including those with musical training) switched to an abnormal dependence on tempo cues. The data indicate that, in a western culture, access to acoustic hearing in early life promotes a preference for mode rather than tempo cues which is enhanced by musical training. The challenge to these preferred strategies during cochlear implant hearing (simulated and real), regardless of musical training, suggests that access to pitch cues for children with hearing loss must be improved by preservation of residual hearing and improvements in cochlear implant technology.     

Music in Our Ears: The Biological Bases of Musical Timbre Perception

Timbre is the attribute of sound that allows humans and other animals to distinguish among different sound sources. Studies based on psychophysical judgments of musical timbre, ecological analyses of sound''s physical characteristics as well as machine learning approaches have all suggested that timbre is a multifaceted attribute that invokes both spectral and temporal sound features. Here, we explored the neural underpinnings of musical timbre. We used a neuro-computational framework based on spectro-temporal receptive fields, recorded from over a thousand neurons in the mammalian primary auditory cortex as well as from simulated cortical neurons, augmented with a nonlinear classifier. The model was able to perform robust instrument classification irrespective of pitch and playing style, with an accuracy of 98.7%. Using the same front end, the model was also able to reproduce perceptual distance judgments between timbres as perceived by human listeners. The study demonstrates that joint spectro-temporal features, such as those observed in the mammalian primary auditory cortex, are critical to provide the rich-enough representation necessary to account for perceptual judgments of timbre by human listeners, as well as recognition of musical instruments.     

Neural substrates of processing syntax and semantics in music

Growing evidence indicates that syntax and semantics are basic aspects of music. After the onset of a chord, initial music-syntactic processing can be observed at about 150-400 ms and processing of musical semantics at about 300-500 ms. Processing of musical syntax activates inferior frontolateral cortex, ventrolateral premotor cortex and presumably the anterior part of the superior temporal gyrus. These brain structures have been implicated in sequencing of complex auditory information, identification of structural relationships, and serial prediction. Processing of musical semantics appears to activate posterior temporal regions. The processes and brain structures involved in the perception of syntax and semantics in music have considerable overlap with those involved in language perception, underlining intimate links between music and language in the human brain.     

Altered low-γ sampling in auditory cortex accounts for the three main facets of dyslexia

It has recently been conjectured that dyslexia arises from abnormal auditory sampling. What sampling rate is altered and how it affects reading remains unclear. We hypothesized that by impairing phonemic parsing abnormal low-gamma sampling could yield phonemic representations of unusual format and disrupt phonological processing and verbal memory. Using magnetoencephalography and behavioral tests, we show in dyslexic subjects a reduced left-hemisphere bias for phonemic processing, reflected in less entrainment to ≈30?Hz acoustic modulations in left auditory cortex. This deficit correlates with measures of phonological processing and rapid naming. We further observed enhanced cortical entrainment at rates beyond 40?Hz in dyslexics and show that this particularity is associated with a verbal memory deficit. These data suggest that a single auditory anomaly, i.e., phonemic oversampling in left auditory cortex, accounts for three main facets of the linguistic deficit in dyslexia.     

Dopaminergic and Serotonergic Neurotransmission Systems Are Differentially Involved in Auditory Cortex Learning: A Long-Term Microdialysis Study of Metabolites

Abstract: Auditory cortex has been shown to be a site of widespread neuronal learning processes even in the context of simple auditory conditioning behavior. In view of their presumed role in determining behavioral and motivational relevance of incoming information we investigated whether the dopaminergic and serotonergic systems are involved in auditory cortex learning. Using a chronic brain microdialysis technique over 4 days, samples from auditory cortex were obtained before, during, and after daily footshock avoidance training simultaneously from trained gerbils and passive control animals or pseudotrained animals. Because of detection limits of dopamine and serotonin in auditory cortex, the response profiles of extracellular homovanillic acid as the metabolite of the dopaminergic system and of 5-hydroxyindoleacetic acid as the metabolite of the serotonergic system were determined from consecutive dialysis samples each day. The response of the dopaminergic system appeared to reflect the initial formation of the behaviorally relevant association exclusively during the first training day, whereas the serotonergic response appeared to correlate with the stress level of animals.     

Diminished behavioral and neural sensitivity to sound modulation is associated with moderate developmental hearing loss

The acoustic rearing environment can alter central auditory coding properties, yet altered neural coding is seldom linked with specific deficits to adult perceptual skills. To test whether developmental hearing loss resulted in comparable changes to perception and sensory coding, we examined behavioral and neural detection thresholds for sinusoidally amplitude modulated (sAM) stimuli. Behavioral sAM detection thresholds for slow (5 Hz) modulations were significantly worse for animals reared with bilateral conductive hearing loss (CHL), as compared to controls. This difference could not be attributed to hearing thresholds, proficiency at the task, or proxies for attention. Detection thresholds across the groups did not differ for fast (100 Hz) modulations, a result paralleling that seen in humans. Neural responses to sAM stimuli were recorded in single auditory cortex neurons from separate groups of awake animals. Neurometric analyses indicated equivalent thresholds for the most sensitive neurons, but a significantly poorer detection threshold for slow modulations across the population of CHL neurons as compared to controls. The magnitude of the neural deficit matched that of the behavioral differences, suggesting that a reduction of sensory information can account for limitations to perceptual skills.     

Fractionating the musical mind: insights from congenital amusia

Music, like language, is acquired effortlessly in early life and fulfils a multitude of social, cultural and emotional functions. However, those with a disorder recently termed 'congenital amusia' (CA) fail to recognise common tunes from their culture, do not hear when notes are 'out of tune' and sometimes report that music sounds like a 'din' or 'banging'. The core deficit appears to be a problem in discriminating pitch direction, a building block for the representation of melodic contour. Familial studies suggest the disorder is heritable and associated with structural differences in temporal and frontal cortices. The disorder provides a window onto the neuro-cognitive architecture of musical processing, and the possible etiologies of disordered development.     

Audio-Tactile Integration and the Influence of Musical Training

Perception of our environment is a multisensory experience; information from different sensory systems like the auditory, visual and tactile is constantly integrated. Complex tasks that require high temporal and spatial precision of multisensory integration put strong demands on the underlying networks but it is largely unknown how task experience shapes multisensory processing. Long-term musical training is an excellent model for brain plasticity because it shapes the human brain at functional and structural levels, affecting a network of brain areas. In the present study we used magnetoencephalography (MEG) to investigate how audio-tactile perception is integrated in the human brain and if musicians show enhancement of the corresponding activation compared to non-musicians. Using a paradigm that allowed the investigation of combined and separate auditory and tactile processing, we found a multisensory incongruency response, generated in frontal, cingulate and cerebellar regions, an auditory mismatch response generated mainly in the auditory cortex and a tactile mismatch response generated in frontal and cerebellar regions. The influence of musical training was seen in the audio-tactile as well as in the auditory condition, indicating enhanced higher-order processing in musicians, while the sources of the tactile MMN were not influenced by long-term musical training. Consistent with the predictive coding model, more basic, bottom-up sensory processing was relatively stable and less affected by expertise, whereas areas for top-down models of multisensory expectancies were modulated by training.     

听觉选择性注意的可塑性及其神经机制研究

本文旨在研究音乐训练是否能增强基于音高和空间位置的听觉选择性注意力,以及音乐训练对听觉可塑性的神经机制.听觉感知实验中,受试者根据音高差异或空间位置差异,选择两个同时播放的数字之一.听觉认知实验在安静和噪声环境中播放频率分辨率不同的复合音,记录受试者听觉脑干频率跟随响应(frequency-following responses,FFRs).本文提出分析FFR的四种方法,即包络相关频率跟随响应(envelope-related frequency-following response,FFRENV)的短时锁相值、瞬时相位差极性图、相位差均值矢量以及时间细节结构相关频率跟随响应(temporal-fine-structure-related frequency-following response,FFRTFS)的幅度谱信噪比.实验结果表明,在完成基于音高的任务时,受过音乐训练的受试者准确率更高、反应时间更短.外界噪声不影响两组人群在基频(fundamental frequency,F0)的神经元锁相能力,但是显著降低了谐波处的神经元锁相能力.受过音乐训练的受试者的神经元在基频处的锁相能力和谐波处抗噪能力均增强,且其FFRTFS幅度谱信噪比与基于音高的行为学准确率呈正相关.因此,受过音乐训练的受试者其音高选择性注意感知能力的提高取决于认知神经能力的增强,经过音乐训练后,F0处FFRENV的锁相能力、谐波处FFRTFS的抗噪和持续锁相能力以及谐波处FFRTFS幅度谱信噪比均明显增强.音乐训练对听觉选择性注意具有显著的可塑性.