Vinod Menon, Postdoctoral Faculty Sponsor
Musical expertise shapes functional and structural brain networks independent of absolute pitch ability.
The Journal of neuroscience : the official journal of the Society for Neuroscience
Professional musicians are a popular model for investigating experience-dependent plasticity in human large-scale brain networks. A minority of musicians possess absolute pitch, the ability to name a tone without reference. The study of absolute pitch musicians provides insights into how a very specific talent is reflected in brain networks. Previous studies of the effects of musicianship and absolute pitch on large-scale brain networks have yielded highly heterogeneous findings regarding the localization and direction of the effects. This heterogeneity was likely influenced by small samples and vastly different methodological approaches. Here, we conducted a comprehensive multimodal assessment of effects of musicianship and absolute pitch on intrinsic functional and structural connectivity using a variety of commonly employed and state-of-the-art multivariate methods in the largest sample to date (n = 153 female and male human participants; 52 absolute pitch musicians, 51 non-absolute pitch musicians, and 50 non-musicians). Our results show robust effects of musicianship in inter- and intrahemispheric connectivity in both structural and functional networks. Crucially, most of the effects were replicable in both musicians with and without absolute pitch when compared to non-musicians. However, we did not find evidence for an effect of absolute pitch on intrinsic functional or structural connectivity in our data: The two musician groups showed strikingly similar networks across all analyses. Our results suggest that long-term musical training is associated with robust changes in large-scale brain networks. The effects of absolute pitch on neural networks might be subtle, requiring very large samples or task-based experiments to be detected.SIGNIFICANCE STATEMENT A question that has fascinated neuroscientists, psychologists, and musicologists for a long time is how musicianship and absolute pitch, the rare talent to name a tone without reference, are reflected in large-scale networks of the human brain. Much is still unknown as previous studies have reported widely inconsistent results based on small samples. Here, we investigate the largest sample of musicians and non-musicians to date (n = 153) using a multitude of established and novel analysis methods. Results provide evidence for robust effects of musicianship on functional and structural networks that were replicable in two separate groups of musicians and independent of absolute pitch ability.
View details for DOI 10.1523/JNEUROSCI.1985-20.2020
View details for PubMedID 33495199
Heterogeneity of EEG resting-state brain networks in absolute pitch.
International journal of psychophysiology : official journal of the International Organization of Psychophysiology
The neural basis of absolute pitch (AP), the ability to effortlessly identify a musical tone without an external reference, is poorly understood. One of the key questions is whether perceptual or cognitive processes underlie the phenomenon as both sensory and higher-order brain regions have been associated with AP. To integrate the perceptual and cognitive views on AP, here, we investigated joint contributions of sensory and higher-order brain regions to AP resting-state networks. We performed a comprehensive functional network analysis of source-level EEG in a large sample of AP musicians (n = 54) and non-AP musicians (n = 51), adopting two analysis approaches: First, we applied an ROI-based analysis to examine the connectivity between the auditory cortex and the dorsolateral prefrontal cortex (DLPFC) using several established functional connectivity measures. This analysis is a replication of a previous study which reported increased connectivity between these two regions in AP musicians. Second, we performed a whole-brain network-based analysis on the same functional connectivity measures to gain a more complete picture of the brain regions involved in a possibly large-scale network supporting AP ability. In our sample, the ROI-based analysis did not provide evidence for an AP-specific connectivity increase between the auditory cortex and the DLPFC. The whole-brain analysis revealed three networks with increased connectivity in AP musicians comprising nodes in frontal, temporal, subcortical, and occipital areas. Commonalities of the networks were found in both sensory and higher-order brain regions of the perisylvian area. Further research will be needed to confirm these exploratory results.
View details for DOI 10.1016/j.ijpsycho.2020.07.007
View details for PubMedID 32721558
Diminished large-scale functional brain networks in absolute pitch during the perception of naturalistic music and audiobooks.
Previous studies have reported the effects of absolute pitch (AP) and musical proficiency on the functioning of specific brain regions or distinct subnetworks, but they provided an incomplete account of effects of AP and musical proficiency on whole-brain networks. In this study, we used EEG to estimate source-space whole-brain functional connectivity in a large sample comprising AP musicians (n = 46), relative pitch (RP) musicians (n = 45), and Non-musicians (n = 34) during resting state, naturalistic music listening, and audiobook listening. First, we assessed the global network density of the participants' functional networks in these conditions. As revealed by cluster-based permutation testing, AP musicians showed a decreased mean degree compared to Non-musicians whereas RP musicians showed an intermediate mean degree not statistically different from Non-musicians or AP-musicians. This effect was present during naturalistic music and audiobook listening, but, crucially, not during resting state. Second, we identified subnetworks that drive group differences in global network density using the network-based statistic approach. We found that AP musicians showed decreased functional connectivity in major hubs of the default mode network during both music and audiobook listening compared to Non-musicians. Third, we assessed group differences in global network topology while controlling for network density. We did not find evidence for group differences in the clustering coefficient and characteristic path length. Taken together, we found first evidence of diminished whole-brain functional networks in AP musicians during the perception of naturalistic auditory stimuli. These differences might reflect a complex interplay between AP ability, musical proficiency, music processing, and auditory processing per se.
View details for DOI 10.1016/j.neuroimage.2019.116513
View details for PubMedID 31901419
Takotsubo syndrome: How the broken heart deals with negative emotions.
2019; 25: 102124
OBJECTIVES: Patients suffering from Takotsubo syndrome have a higher prevalence of anxiety and depressive disorders compared to those with acute myocardial infarction and might thus show impaired regulation and processing of emotions.METHODS: In this cross-sectional study, neural activity during an emotional picture processing task was examined in 26 Takotsubo patients (on average 27 months after the Takotsubo event) and 22 healthy age- and gender-matched control subjects undergoing functional magnetic resonance imaging. Imaging data were analyzed with two complementary approaches: First, univariate analysis was used to detect brain regions showing condition-specific differences in mean neural activity between groups. Second, multivariate pattern analysis was applied to decode the experimental conditions from individual activity patterns.RESULTS: In the univariate analysis approach, patients showed lower bilateral superior parietal activity during the processing of negative expected pictures compared to the control subjects. The multivariate pattern analysis revealed group differences in decoding negative versus neutral pictures from a widespread network consisting of frontal, parietal, occipital, and cerebellar brain regions. Additionally, differences in decoding the expectation of a negative versus positive upcoming picture were observed in the visual cortex.CONCLUSION: The lower involvement of brain regions observed in Takotsubo patients suggests an impairment in emotion regulation, which might be of etiological importance in this brain-heart disease.
View details for DOI 10.1016/j.nicl.2019.102124
View details for PubMedID 31884222
Neural patterns reveal single-trial information on absolute pitch and relative pitch perception
2019; 200: 132–41
Pitch is a fundamental attribute of sounds and yet is not perceived equally by all humans. Absolute pitch (AP) musicians perceive, recognize, and name pitches in absolute terms, whereas relative pitch (RP) musicians, representing the large majority of musicians, perceive pitches in relation to other pitches. In this study, we used electroencephalography (EEG) to investigate the neural representations underlying tone listening and tone labeling in a large sample of musicians (n = 105). Participants performed a pitch processing task with a listening and a labeling condition during EEG acquisition. Using a brain-decoding framework, we tested a prediction derived from both theoretical and empirical accounts of AP, namely that the representational similarity of listening and labeling is higher in AP musicians than in RP musicians. Consistent with the prediction, time-resolved single-trial EEG decoding revealed a higher representational similarity in AP musicians during late stages of pitch perception. Time-frequency-resolved EEG decoding further showed that the higher representational similarity was present in oscillations in the theta and beta frequency bands. Supplemental univariate analyses were less sensitive in detecting subtle group differences in the frequency domain. Taken together, the results suggest differences between AP and RP musicians in late pitch processing stages associated with cognition, rather than in early processing stages associated with perception.
View details for DOI 10.1016/j.neuroimage.2019.06.030
View details for Web of Science ID 000481579300011
View details for PubMedID 31238164
- Perception and Cognition in Absolute Pitch: Distinct yet Inseparable JOURNAL OF NEUROSCIENCE 2019; 39 (30): 5839–41
Absolute and relative pitch processing in the human brain: neural and behavioral evidence
BRAIN STRUCTURE & FUNCTION
2019; 224 (5): 1723–38
Pitch is a primary perceptual dimension of sounds and is crucial in music and speech perception. When listening to melodies, most humans encode the relations between pitches into memory using an ability called relative pitch (RP). A small subpopulation, almost exclusively musicians, preferentially encode pitches using absolute pitch (AP): the ability to identify the pitch of a sound without an external reference. In this study, we recruited a large sample of musicians with AP (AP musicians) and without AP (RP musicians). The participants performed a pitch-processing task with a Listening and a Labeling condition during functional magnetic resonance imaging. General linear model analysis revealed that while labeling tones, AP musicians showed lower blood oxygenation level-dependent (BOLD) signal in the inferior frontal gyrus and the presupplementary motor area-brain regions associated with working memory, language functions, and auditory imagery. At the same time, AP musicians labeled tones more accurately suggesting that AP might be an example of neural efficiency. In addition, using multivariate pattern analysis, we found that BOLD signal patterns in the inferior frontal gyrus and the presupplementary motor area differentiated between the groups. These clusters were similar, but not identical compared to the general linear model-based clusters. Therefore, information about AP and RP might be present on different spatial scales. While listening to tones, AP musicians showed increased BOLD signal in the right planum temporale which may reflect the matching of pitch information with internal templates and corroborates the importance of the planum temporale in AP processing. Taken together, AP and RP musicians show diverging frontal activations during Labeling and, more subtly, differences in right auditory activation during Listening. The results of this study do not support the previously reported importance of the dorsolateral prefrontal cortex in associating a pitch with its label.
View details for DOI 10.1007/s00429-019-01872-2
View details for Web of Science ID 000471236200003
View details for PubMedID 30968240
Univariate and multivariate analyses of functional networks in absolute pitch
2019; 189: 241–47
Absolute pitch (AP) refers to the rare ability to identify the pitch of any given tone without an external reference tone. Previous studies have shown that during auditory processing, AP musicians activate the auditory cortex (AC), the prefrontal cortex (PFC), and parietal areas of the brain. Therefore, it has been hypothesized that AP is sustained by a widespread functional network. In the present functional magnetic resonance imaging (fMRI) study, we tested this hypothesis by employing a mass-univariate analysis of resting-state functional connectivity within the AC, the PFC, and parietal areas in a large sample of musicians with and without AP (N = 100). AP musicians showed increased functional connectivity in the left middle frontal gyrus (MFG), left intraparietal sulcus (IPS), and right superior parietal lobule (SPL). These results provide the first evidence for an AP-specific network characterized by increased functional connections in higher-order cognitive areas. Interestingly, AP was not associated with increases in functional connectivity of the AC, but AP was successfully decoded from functional connectivity patterns in the left AC using multi-voxel pattern analysis (MVPA, also known as multivariate pattern analysis), with group classification accuracy being highest for the left Heschl's gyrus (HG). MVPA can capture fine-grained patterns in the brain connectivity profile of AP musicians, whilst a mass-univariate analysis is sensitive to macroscopic trends in the data. The successful differentiation of AP musicians by MVPA but not by a mass-univariate analysis of connectivity in the AC thus indicates that AP musicians differ in the fine-grained rather than the macroscopic AC function. Based on our findings, and in light of current literature, we propose pitch-label associations, tonal working memory, pitch categorization, and multimodal integration as potential mechanisms underlying the AP ability. This set of psychological functions is controlled by a distributed functional network and a particular AC connectivity pattern only present in AP musicians.
View details for DOI 10.1016/j.neuroimage.2019.01.021
View details for Web of Science ID 000461166900021
View details for PubMedID 30639332
A reevaluation of the electrophysiological correlates of absolute pitch and relative pitch: No evidence for an absolute pitch-specific negativity
INTERNATIONAL JOURNAL OF PSYCHOPHYSIOLOGY
2019; 137: 21–31
Musicians with absolute pitch effortlessly identify the pitch of a sound without an external reference. Previous neuroscientific studies on absolute pitch have typically had small samples sizes and low statistical power, making them susceptible for false positive findings. In a seminal study, Itoh et al. (2005) reported the elicitation of an absolute pitch-specific event-related potential component during tone listening - the AP negativity. Additionally, they identified several components as correlates of relative pitch, the ability to identify relations between pitches. Here, we attempted to replicate the main findings of Itoh et al.'s study in a large sample of musicians (n = 104) using both frequentist and Bayesian inference. We were not able to replicate the presence of an AP negativity during tone listening in individuals with high levels of absolute pitch, but we partially replicated the findings concerning the correlates of relative pitch. Our results are consistent with several previous studies reporting an absence of differences between musicians with and without absolute pitch in early auditory evoked potential components. We conclude that replication studies form a crucial part in assessing extraordinary findings, even more so in small fields where a single finding can have a large impact on further research.
View details for DOI 10.1016/j.ijpsycho.2018.12.016
View details for Web of Science ID 000459840900003
View details for PubMedID 30610912
The neural underpinnings of music listening under different attention conditions
2018; 29 (7): 594–604
Most studies examining the neural underpinnings of music listening have no specific instruction on how to process the presented musical pieces. In this study, we explicitly manipulated the participants' focus of attention while they listened to the musical pieces. We used an ecologically valid experimental setting by presenting the musical stimuli simultaneously with naturalistic film sequences. In one condition, the participants were instructed to focus their attention on the musical piece (attentive listening), whereas in the second condition, the participants directed their attention to the film sequence (passive listening). We used two instrumental musical pieces: an electronic pop song, which was a major hit at the time of testing, and a classical musical piece. During music presentation, we measured electroencephalographic oscillations and responses from the autonomic nervous system (heart rate and high-frequency heart rate variability). During passive listening to the pop song, we found strong event-related synchronizations in all analyzed frequency bands (theta, lower alpha, upper alpha, lower beta, and upper beta). The neurophysiological responses during attentive listening to the pop song were similar to those of the classical musical piece during both listening conditions. Thus, the focus of attention had a strong influence on the neurophysiological responses to the pop song, but not on the responses to the classical musical piece. The electroencephalographic responses during passive listening to the pop song are interpreted as a neurophysiological and psychological state typically observed when the participants are 'drawn into the music'.
View details for DOI 10.1097/WNR.0000000000001019
View details for Web of Science ID 000430475400013
View details for PubMedID 29596153