Using cortico-cerebellar structural patterns to classify early- and late-trained musicians.

A body of current evidence suggests that there is a sensitive period for musical training: people who begin training before the age of seven show better performance on tests of musical skill, and also show differences in brain structure-especially in motor cortical and cerebellar regions-compared with those who start later. We used support vector machine models-a subtype of supervised machine learning-to investigate distributed patterns of structural differences between early-trained (ET) and late-trained (LT) musicians and to better understand the age boundaries of the sensitive period for early musicianship. After selecting regions of interest from the cerebellum and cortical sensorimotor regions, we applied recursive feature elimination with cross-validation to produce a model which optimally and accurately classified ET and LT musicians. This model identified a combination of 17 regions, including 9 cerebellar and 8 sensorimotor regions, and maintained a high accuracy and sensitivity (true positives, i.e., ET musicians) without sacrificing specificity (true negatives, i.e., LT musicians). Critically, this model-which defined ET musicians as those who began their training before the age of 7-outperformed all other models in which age of start was earlier or later (between ages 5-10). Our model's ability to accurately classify ET and LT musicians provides additional evidence that musical training before age 7 affects cortico-cerebellar structure in adulthood, and is consistent with the hypothesis that connected brain regions interact during development to reciprocally influence brain and behavioral maturation.

Rhythm and time in the premotor cortex.

Many animals can encode temporal intervals and use them to plan their actions, but only humans can flexibly extract a regular beat from complex patterns, such as musical rhythms. Beat-based timing is hypothesized to rely on the integration of sensory information with temporal information encoded in motor regions such as the medial premotor cortex (MPC), but how beat-based timing might be encoded in neuronal populations is mostly unknown. Gámez and colleagues show that the MPC encodes temporal information via a population code visible as circular trajectories in state space; these patterns may represent precursors to more-complex skills such as beat-based timing.

Effector-independent brain network for auditory-motor integration: fMRI evidence from singing and cello playing.

Many everyday tasks share high-level sensory goals but differ in the movements used to accomplish them. One example of this is musical pitch regulation, where the same notes can be produced using the vocal system or a musical instrument controlled by the hands. Cello playing has previously been shown to rely on brain structures within the singing network for performance of single notes, except in areas related to primary motor control, suggesting that the brain networks for auditory feedback processing and sensorimotor integration may be shared (Segado et al. 2018). However, research has shown that singers and cellists alike can continue singing/playing in tune even in the absence of auditory feedback (Chen et al. 2013, Kleber et al. 2013), so different paradigms are required to test feedback monitoring and control mechanisms. In singing, auditory pitch feedback perturbation paradigms have been used to show that singers engage a network of brain regions including anterior cingulate cortex (ACC), anterior insula (aINS), and intraparietal sulcus (IPS) when compensating for altered pitch feedback, and posterior superior temporal gyrus (pSTG) and supramarginal gyrus (SMG) when ignoring it (Zarate et al. 2005, 2008). To determine whether the brain networks for cello playing and singing directly overlap in these sensory-motor integration areas, in the present study expert cellists were asked to compensate for or ignore introduced pitch perturbations when singing/playing during fMRI scanning. We found that cellists were able to sing/play target tones, and compensate for and ignore introduced feedback perturbations equally well. Brain activity overlapped for singing and playing in IPS and SMG when compensating, and pSTG and dPMC when ignoring; differences between singing/playing across all three conditions were most prominent in M1, centered on the relevant motor effectors (hand, larynx). These findings support the hypothesis that pitch regulation during cello playing relies on structures within the singing network and suggests that differences arise primarily at the level of forward motor control.

The sensation of groove engages motor and reward networks.

The sensation of groove has been defined as the pleasurable desire to move to music, suggesting that both motor timing and reward processes are involved in this experience. Although many studies have investigated rhythmic timing and musical reward separately, none have examined whether the associated cortical and subcortical networks are engaged while participants listen to groove-based music. In the current study, musicians and non-musicians listened to and rated experimentally controlled groove-based stimuli while undergoing functional magnetic resonance imaging. Medium complexity rhythms elicited higher ratings of pleasure and wanting to move and were associated with activity in regions linked to beat perception and reward, as well as prefrontal and parietal regions implicated in generating and updating stimuli-based expectations. Activity in basal ganglia regions of interest, including the nucleus accumbens, caudate and putamen, was associated with ratings of pleasure and wanting to move, supporting their important role in the sensation of groove. We propose a model in which different cortico-striatal circuits interact to support the mechanisms underlying groove, including internal generation of the beat, beat-based expectations, and expectation-based affect. These results show that the sensation of groove is supported by motor and reward networks in the brain and, along with our proposed model, suggest that the basal ganglia are crucial nodes in networks that interact to generate this powerful response to music.

Efficacy of Auditory versus Motor Learning for Skilled and Novice Performers.

Humans must learn a variety of sensorimotor skills, yet the relative contributions of sensory and motor information to skill acquisition remain unclear. Here we compare the behavioral and neural contributions of perceptual learning to that of motor learning, and we test whether these contributions depend on the expertise of the learner. Pianists and nonmusicians learned to perform novel melodies on a piano during fMRI scanning in four learning conditions: listening (auditory learning), performing without auditory feedback (motor learning), performing with auditory feedback (auditory-motor learning), or observing visual cues without performing or listening (cue-only learning). Visual cues were present in every learning condition and consisted of musical notation for pianists and spatial cues for nonmusicians. Melodies were performed from memory with no visual cues and with auditory feedback (recall) five times during learning. Pianists showed greater improvements in pitch and rhythm accuracy at recall during auditory learning compared with motor learning. Nonmusicians demonstrated greater rhythm improvements at recall during auditory learning compared with all other learning conditions. Pianists showed greater primary motor response at recall during auditory learning compared with motor learning, and response in this region during auditory learning correlated with pitch accuracy at recall and with auditory-premotor network response during auditory learning. Nonmusicians showed greater inferior parietal response during auditory compared with auditory-motor learning, and response in this region correlated with pitch accuracy at recall. Results suggest an advantage for perceptual learning compared with motor learning that is both general and expertise-dependent. This advantage is hypothesized to depend on feedforward motor control systems that can be used during learning to transform sensory information into motor production.

Auditory prediction cues motor preparation in the absence of movements.

There is increasing evidence for integrated representation of sensory and motor information in the brain, and that seeing or hearing action-related stimuli may automatically cue the movements required to respond to or produce them. In this study we tested whether anticipation of tones in a known melody automatically activates corresponding motor representations in a predictive way, in preparation for potential upcoming movements. Therefore, we trained 20 non-musicians (8 men, 12 women) to play a simple melody. Then, while they passively listened to the learned or unlearned melodies, we applied single pulse transcranial magnetic stimulation (TMS) over M1 to measure motor evoked potentials from the associated finger muscle either preceding or following the onset of individual tones. Our results show that listening to the learned melody increased corticospinal excitability for specific finger muscles before tone onset. This demonstrates that predictable auditory information can activate motor representations in an anticipatory muscle-specific manner, even in the absence of intention to move. This suggests that the motor system is involved in the prediction of sensory events, likely based on auditory-parietal-prefrontal feedforward/feedback loops that automatically prepare predictable sound-related actions independent of actual execution and the associated auditory feedback. Overall, we propose that multimodal forward models of upcoming sounds and actions support motor preparation, facilitate error detection and correction, and guide perception.

Sensorimotor integration is enhanced in dancers and musicians.

Studying individuals with specialized training, such as dancers and musicians, provides an opportunity to investigate how intensive practice of sensorimotor skills affects behavioural performance across various domains. While several studies have found that musicians have improved motor, perceptual and sensorimotor integration skills compared to untrained controls, fewer studies have examined the effect of dance training on such skills. Moreover, no study has specifically compared the effects of dance versus music training on perceptual or sensorimotor performance. To this aim, in the present study, expert dancers, expert musicians and untrained controls were tested on a range of perceptual and sensorimotor tasks designed to discriminate performance profiles across groups. Dancers performed better than musicians and controls on a dance imitation task (involving whole-body movement), but musicians performed better than dancers and controls on a musical melody discrimination task as well as on a rhythm synchronization task (involving finger tapping). These results indicate that long-term intensive dance and music training are associated with distinct enhancements in sensorimotor skills. This novel work advances knowledge of the effects of long-term dance versus music training and has potential applications in therapies for motor disorders.

Effects of age and cognitive load on response reprogramming.

A dual-task paradigm was used to examine the effect of cognitive load on motor reprogramming. We propose that in the face of conflict, both executive control and motor control mechanisms become more interconnected in the process of reprogramming motor behaviors. If so, one would expect a concurrent cognitive load to compromise younger adults' (YAs) motor reprogramming ability and further exacerbate the response reprogramming ability of older adults (OAs). Nineteen YAs and 14 OAs overlearned a sequence of key presses. Deviations of the practiced sequence were introduced to assess motor reprogramming ability. A Serial Sevens Test was used as the cognitive load. A 3D motion capture system was used to parse finger movements into planning and motor execution times. Global response time analysis revealed that under single-task conditions, during prepotent transitions, OAs responded as quickly as YAs, but they were disproportionately worse than YAs during conflict transitions. Under dual-task conditions, YAs performance became more similar to that of OAs. Movement data were decomposed into planning and movement time, revealing that under single-task conditions, when responding to conflicting stimuli YAs reduced their movement time in order to compensate for delayed planning time; however, additional cognitive load prevented them from exhibiting this compensatory hastening on conflict transitions. We propose that age-related declines in response reprogramming may be linked to reduced cognitive capacity. Current findings suggest that cognitive capacity, reduced in the case of OAs or YAs under divided attention conditions, influences the ability to flexibly adapt to conflicting conditions.

Early musical training and white-matter plasticity in the corpus callosum: evidence for a sensitive period.

Training during a sensitive period in development may have greater effects on brain structure and behavior than training later in life. Musicians are an excellent model for investigating sensitive periods because training starts early and can be quantified. Previous studies suggested that early training might be related to greater amounts of white matter in the corpus callosum, but did not control for length of training or identify behavioral correlates of structural change. The current study compared white-matter organization using diffusion tensor imaging in early- and late-trained musicians matched for years of training and experience. We found that early-trained musicians had greater connectivity in the posterior midbody/isthmus of the corpus callosum and that fractional anisotropy in this region was related to age of onset of training and sensorimotor synchronization performance. We propose that training before the age of 7 years results in changes in white-matter connectivity that may serve as a scaffold upon which ongoing experience can build.

Early musical training is linked to gray matter structure in the ventral premotor cortex and auditory-motor rhythm synchronization performance.

Evidence in animals and humans indicates that there are sensitive periods during development, times when experience or stimulation has a greater influence on behavior and brain structure. Sensitive periods are the result of an interaction between maturational processes and experience-dependent plasticity mechanisms. Previous work from our laboratory has shown that adult musicians who begin training before the age of 7 show enhancements in behavior and white matter structure compared with those who begin later. Plastic changes in white matter and gray matter are hypothesized to co-occur; therefore, the current study investigated possible differences in gray matter structure between early-trained (ET; <7) and late-trained (LT; >7) musicians, matched for years of experience. Gray matter structure was assessed using voxel-wise analysis techniques (optimized voxel-based morphometry, traditional voxel-based morphometry, and deformation-based morphometry) and surface-based measures (cortical thickness, surface area and mean curvature). Deformation-based morphometry analyses identified group differences between ET and LT musicians in right ventral premotor cortex (vPMC), which correlated with performance on an auditory motor synchronization task and with age of onset of musical training. In addition, cortical surface area in vPMC was greater for ET musicians. These results are consistent with evidence that premotor cortex shows greatest maturational change between the ages of 6-9 years and that this region is important for integrating auditory and motor information. We propose that the auditory and motor interactions required by musical practice drive plasticity in vPMC and that this plasticity is greatest when maturation is near its peak.

Interacting cortical and basal ganglia networks underlying finding and tapping to the musical beat.

Humans are able to find and tap to the beat of musical rhythms varying in complexity from children's songs to modern jazz. Musical beat has no one-to-one relationship with auditory features-it is an abstract perceptual representation that emerges from the interaction between sensory cues and higher-level cognitive organization. Previous investigations have examined the neural basis of beat processing but have not tested the core phenomenon of finding and tapping to the musical beat. To test this, we used fMRI and had musicians find and tap to the beat of rhythms that varied from metrically simple to metrically complex-thus from a strong to a weak beat. Unlike most previous studies, we measured beat tapping performance during scanning and controlled for possible effects of scanner noise on beat perception. Results showed that beat finding and tapping recruited largely overlapping brain regions, including the superior temporal gyrus (STG), premotor cortex, and ventrolateral PFC (VLPFC). Beat tapping activity in STG and VLPFC was correlated with both perception and performance, suggesting that they are important for retrieving, selecting, and maintaining the musical beat. In contrast BG activity was similar in all conditions and was not correlated with either perception or production, suggesting that it may be involved in detecting auditory temporal regularity or in associating auditory stimuli with a motor response. Importantly, functional connectivity analyses showed that these systems interact, indicating that more basic sensorimotor mechanisms instantiated in the BG work in tandem with higher-order cognitive mechanisms in PFC.

Repetition suppression in auditory-motor regions to pitch and temporal structure in music.

Music performance requires control of two sequential structures: the ordering of pitches and the temporal intervals between successive pitches. Whether pitch and temporal structures are processed as separate or integrated features remains unclear. A repetition suppression paradigm compared neural and behavioral correlates of mapping pitch sequences and temporal sequences to motor movements in music performance. Fourteen pianists listened to and performed novel melodies on an MR-compatible piano keyboard during fMRI scanning. The pitch or temporal patterns in the melodies either changed or repeated (remained the same) across consecutive trials. We expected decreased neural response to the patterns (pitch or temporal) that repeated across trials relative to patterns that changed. Pitch and temporal accuracy were high, and pitch accuracy improved when either pitch or temporal sequences repeated over trials. Repetition of either pitch or temporal sequences was associated with linear BOLD decrease in frontal-parietal brain regions including dorsal and ventral premotor cortex, pre-SMA, and superior parietal cortex. Pitch sequence repetition (in contrast to temporal sequence repetition) was associated with linear BOLD decrease in the intraparietal sulcus (IPS) while pianists listened to melodies they were about to perform. Decreased BOLD response in IPS also predicted increase in pitch accuracy only when pitch sequences repeated. Thus, behavioral performance and neural response in sensorimotor mapping networks were sensitive to both pitch and temporal structure, suggesting that pitch and temporal structure are largely integrated in auditory-motor transformations. IPS may be involved in transforming pitch sequences into spatial coordinates for accurate piano performance.

Context changes judgments of liking and predictability for melodies.

Predictability plays an important role in the experience of musical pleasure. By leveraging expectations, music induces pleasure through tension and surprise. However, musical predictions draw on both prior knowledge and immediate context. Similarly, musical pleasure, which has been shown to depend on predictability, may also vary relative to the individual and context. Although research has demonstrated the influence of both long-term knowledge and stimulus features in influencing expectations, it is unclear how perceptions of a melody are influenced by comparisons to other music pieces heard in the same context. To examine the effects of context we compared how listeners' judgments of two distinct sets of stimuli differed when they were presented alone or in combination. Stimuli were excerpts from a repertoire of Western music and a set of experimenter created melodies. Separate groups of participants rated liking and predictability for each set of stimuli alone and in combination. We found that when heard together, the Repertoire stimuli were more liked and rated as less predictable than if they were heard alone, with the opposite pattern being observed for the Experimental stimuli. This effect was driven by a change in ratings between the Alone and Combined conditions for each stimulus set. These findings demonstrate a context-based shift of predictability ratings and derived pleasure, suggesting that judgments stem not only from the physical properties of the stimulus, but also vary relative to other options available in the immediate context.

Understanding Sensitive Period Effects in Musical Training.

Adult ability in complex cognitive domains, including music, is commonly thought of as the product of gene-environment interactions, where genetic predispositions influence and are modulated by experience, resulting in the final phenotypic expression. Recently, however, the important contribution of maturation to gene-environment interactions has become better understood. Thus, the timing of exposure to specific experience, such as music training, has been shown to produce long-term impacts on adult behaviour and the brain. Work from our lab and others shows that musical training before the ages of 7-9 enhances performance on musical tasks and modifies brain structure and function, sometimes in unexpected ways. The goal of this paper is to present current evidence for sensitive period effects for musical training in the context of what is known about brain maturation and to present a framework that integrates genetic, environmental and maturational influences on the development of musical skill. We believe that this framework can also be applied more broadly to understanding how predispositions, brain development and experience interact.

Early musical training shapes cortico-cerebellar structural covariation.

Adult abilities in complex cognitive domains such as music appear to depend critically on the age at which training or experience begins, and relevant experience has greater long-term effects during periods of peak maturational change. Previous work has shown that early trained musicians (ET; < age 7) out-perform later-trained musicians (LT; > age 7) on tests of musical skill, and also have larger volumes of the ventral premotor cortex (vPMC) and smaller volumes of the cerebellum. These cortico-cerebellar networks mature and function in relation to one another, suggesting that early training may promote coordinated developmental plasticity. To test this hypothesis, we examined structural covariation between cerebellar volume and cortical thickness (CT) in sensorimotor regions in ET and LT musicians and non-musicians (NMs). Results show that ETs have smaller volumes in cerebellar lobules connected to sensorimotor cortices, while both musician groups had greater cortical thickness in right pre-supplementary motor area (SMA) and right PMC compared to NMs. Importantly, early musical training had a specific effect on structural covariance between the cerebellum and cortex: NMs showed negative correlations between left lobule VI and right pre-SMA and PMC, but this relationship was reduced in ET musicians. ETs instead showed a significant negative correlation between vermal IV and right pre-SMA and dPMC. Together, these results suggest that early musical training has differential impacts on the maturation of cortico-cerebellar networks important for optimizing sensorimotor performance. This conclusion is consistent with the hypothesis that connected brain regions interact during development to reciprocally influence brain and behavioral maturation.

Specific increases within global decreases: a functional magnetic resonance imaging investigation of five days of motor sequence learning.

Our capacity to learn movement sequences is fundamental to our ability to interact with the environment. Although different brain networks have been linked with different stages of learning, there is little evidence for how these networks change across learning. We used functional magnetic resonance imaging to identify the specific contributions of the cerebellum and primary motor cortex (M1) during early learning, consolidation, and retention of a motor sequence task. Performance was separated into two components: accuracy (the more explicit, rapidly learned, stimulus-response association component) and synchronization (the more procedural, slowly learned component). The network of brain regions active during early learning was dominated by the cerebellum, premotor cortex, basal ganglia, presupplementary motor area, and supplementary motor area as predicted by existing models. Across days of learning, as performance improved, global decreases were found in the majority of these regions. Importantly, within the context of these global decreases, we found specific regions of the left M1 and right cerebellar VIIIA/VIIB that were positively correlated with improvements in synchronization performance. Improvements in accuracy were correlated with increases in hippocampus, BA 9/10, and the putamen. Thus, the two behavioral measures, accuracy and synchrony, were found to be related to two different sets of brain regions-suggesting that these networks optimize different components of learning. In addition, M1 activity early on day 1 was shown to be predictive of the degree of consolidation on day 2. Finally, functional connectivity between M1 and cerebellum in late learning points to their interaction as a mechanism underlying the long-term representation and expression of a well learned skill.

Rhythm synchronization performance and auditory working memory in early- and late-trained musicians.

Behavioural and neuroimaging studies provide evidence for a possible "sensitive" period in childhood development during which musical training results in long-lasting changes in brain structure and auditory and motor performance. Previous work from our laboratory has shown that adult musicians who begin training before the age of 7 (early-trained; ET) perform better on a visuomotor task than those who begin after the age of 7 (late-trained; LT), even when matched on total years of musical training and experience. Two questions were raised regarding the findings from this experiment. First, would this group performance difference be observed using a more familiar, musically relevant task such as auditory rhythms? Second, would cognitive abilities mediate this difference in task performance? To address these questions, ET and LT musicians, matched on years of musical training, hours of current practice and experience, were tested on an auditory rhythm synchronization task. The task consisted of six woodblock rhythms of varying levels of metrical complexity. In addition, participants were tested on cognitive subtests measuring vocabulary, working memory and pattern recognition. The two groups of musicians differed in their performance of the rhythm task, such that the ET musicians were better at reproducing the temporal structure of the rhythms. There were no group differences on the cognitive measures. Interestingly, across both groups, individual task performance correlated with auditory working memory abilities and years of formal training. These results support the idea of a sensitive period during the early years of childhood for developing sensorimotor synchronization abilities via musical training.

The effect of practice pattern on the acquisition, consolidation, and transfer of visual-motor sequences.

The contextual interference hypothesis proposes that when learning multiple skills, massing practice leads to better within-day acquisition, whereas random practice leads to better retention and transfer. In this experiment, we examined the effect of practice pattern on the learning, consolidation (retention), and transfer of visual-motor sequences. On Day 1, participants were randomly assigned to the Massed, Alternating, or Random condition. On Day 2, all participants were tested for consolidation and transfer. Learning was assessed through changes in accuracy and response synchronization. We found that massed practice led to enhanced sensorimotor integration and timing (as measured by response synchronization), whereas random practice led to better stimulus-response association (as measured by accuracy). On day 2, all groups showed consolidation for both measures, as well as transfer for accuracy but not response synchronization. Overall, this pattern of results provides limited support for the contextual interference hypothesis. Our findings are consistent with differential encoding of specific domains of motor performance. We propose that learning of the more explicit stimulus-response association is a fast process that benefits from random practice because it requires the acquisition of this association in multiple contexts. Once the association is learned, it seems resistant to interference and transferrable to a novel sequence. In contrast, learning of the sensorimotor integration and timing is a slower process that benefits from blocked training because practice in a single context allows fine-tuning of the response. Given that all groups showed consolidation, we postulate that learning that occurs in the context of interference can show consolidation.

Gesture imitation in musicians and non-musicians.

Imitation plays a crucial role in the learning of many complex motor skills. Recent behavioral and neuroimaging evidence suggests that the ability to imitate is influenced by past experience, such as musical training. To investigate the impact of musical training on motor imitation, musicians and non-musicians were tested on their ability to imitate videoclips of simple and complex two-handed gestures taken from American Sign Language. Participants viewed a set of 30 gestures, one at a time, and imitated them immediately after presentation. Participants' imitations were videotaped and scored off-line by raters blind to participant group. Imitation performance was assessed by a rating of performance accuracy, where the arm, hand, and finger components of the gestures were rated separately on a 5-point scale (1 = unrecognizable; 5 = exact imitation). A global accuracy score (PAglobal) was calculated by summing the three components. Response duration compared to the model (%MTdiff), and reaction time (RT) were also assessed. Results indicated that musicians were able to imitate more accurately than non-musicians, reflected by significantly higher PAglobal and lower %MTdiff scores. Furthermore, the greatest difference in performance was for the fine-motor (finger) gesture component. These findings support the view that the ability to imitate is influenced by experience. This is consistent with generalist theories of motor imitation, which explain imitation in terms of links between perceptual and motor action representations that become strengthened through experience. It is also likely that musical training contributed to the ability to imitate manual gestures by influencing the personal action repertoire of musicians.