María Herrojo Ruiz

Unsupervised statistical learning underpins computational, behavioural, and neural manifestations of musical expectation

The ability to anticipate forthcoming events has clear evolutionary advantages, and predictive successes or failures often entail significant psychological and physiological consequences. In music perception, the confirmation and violation of expectations are critical to the communication of emotion and aesthetic effects of a composition. Neuroscientific research on musical expectations has focused on harmony. Although harmony is important in Western tonal styles, other musical traditions, emphasizing pitch and melody, have been rather neglected. In this study, we investigated melodic pitch expectations elicited by ecologically valid musical stimuli by drawing together computational, behavioural, and electrophysiological evidence. Unlike rule-based models, our computational model acquires knowledge through unsupervised statistical learning of sequential structure in music and uses this knowledge to estimate the conditional probability (and information content) of musical notes. Unlike previous behavioural paradigms that interrupt a stimulus, we devised a new paradigm for studying auditory expectation without compromising ecological validity. A strong negative correlation was found between the probability of notes predicted by our model and the subjectively perceived degree of expectedness. Our electrophysiological results showed that low-probability notes, as compared to high-probability notes, elicited a larger (i) negative ERP component at a late time period (400-450 ms), (ii) beta band (14-30 Hz) oscillation over the parietal lobe, and (iii) long-range phase synchronization between multiple brain regions. Altogether, the study demonstrated that statistical learning produces information-theoretic descriptions of musical notes that are proportional to their perceived expectedness and are associated with characteristic patterns of neural activity.

Detecting Wrong Notes in Advance: Neuronal Correlates of Error Monitoring in Pianists

Music performance is an extremely rapid process with low incidence of errors even at the fast rates of production required. This is possible only due to the fast functioning of the self-monitoring system. Surprisingly, no specific data about error monitoring have been published in the music domain. Consequently, the present study investigated the electrophysiological correlates of executive control mechanisms, in particular error detection, during piano performance. Our target was to extend the previous research efforts on understanding of the human action-monitoring system by selecting a highly skilled multimodal task. Pianists had to retrieve memorized music pieces at a fast tempo in the presence or absence of auditory feedback. Our main interest was to study the interplay between auditory and sensorimotor information in the processes triggered by an erroneous action, considering only wrong pitches as errors. We found that around 70 ms prior to errors a negative component is elicited in the event-related potentials and is generated by the anterior cingulate cortex. Interestingly, this component was independent of the auditory feedback. However, the auditory information did modulate the processing of the errors after their execution, as reflected in a larger error positivity (Pe). Our data are interpreted within the context of feedforward models and the auditory-motor coupling.

EEG oscillatory patterns are associated with error prediction during music performance and are altered in musician's dystonia

Skilled performance requires the ability to monitor ongoing behavior, detect errors in advance and modify the performance accordingly. The acquisition of fast predictive mechanisms might be possible due to the extensive training characterizing expertise performance. Recent EEG studies on piano performance reported a negative event-related potential (ERP) triggered in the ACC 70 ms before performance errors (pitch errors due to incorrect keypress). This ERP component, termed pre-error related negativity (pre-ERN), was assumed to reflect processes of error detection in advance. However, some questions remained to be addressed: (i) Does the electrophysiological marker prior to errors reflect an error signal itself or is it related instead to the implementation of control mechanisms? (ii) Does the posterior frontomedial cortex (pFMC, including ACC) interact with other brain regions to implement control adjustments following motor prediction of an upcoming error? (iii) Can we gain insight into the electrophysiological correlates of error prediction and control by assessing the local neuronal synchronization and phase interaction among neuronal populations? (iv) Finally, are error detection and control mechanisms defective in pianists with musicians dystonia (MD), a focal task-specific dystonia resulting from dysfunction of the basal ganglia-thalamic-frontal circuits? Consequently, we investigated the EEG oscillatory and phase synchronization correlates of error detection and control during piano performances in healthy pianists and in a group of pianists with MD. In healthy pianists, the main outcomes were increased pre-error theta and beta band oscillations over the pFMC and 13-15 Hz phase synchronization, between the pFMC and the right lateral prefrontal cortex, which predicted corrective mechanisms. In MD patients, the pattern of phase synchronization appeared in a different frequency band (6-8 Hz) and correlated with the severity of the disorder. The present findings shed new light on the neural mechanisms, which might implement motor prediction by means of forward control processes, as they function in healthy pianists and in their altered form in patients with MD.

Defective Inhibition and Inter-Regional Phase Synchronization in Pianists With Musician's Dystonia: An EEG Study

Recent neurophysiological studies have associated focal‐task specific dystonia (FTSD) with impaired inhibitory function. However, it remains unknown whether FTSD also affects the inhibition (INH) of long‐term overlearned motor programs. Consequently, we investigated in a Go/NoGo paradigm the neural correlates associated with the activation (ACT) and inhibition of long‐term overlearned motor memory traces in pianists with musicians dystonia (MD), a form of FTSD, during a relevant motor task under constraint timing conditions with multichannel EEG. In NoGo trials, the movement related cortical potentials showed a positive shift after the NoGo signal related to inhibition and was significantly smaller over sensorimotor areas in musicians with MD. Further, we observed an increase at 850–900 ms in the power of beta oscillations which was significantly weaker for the patient group. The role of the inter‐electrode phase coupling in the sensorimotor integration of inhibitory processes turned out to be the most relevant physiological marker: the global phase synchronization during INH exhibited an increase between 230 and 330 ms and 7–8 Hz, increase which was significantly smaller for pianists with MD. This effect was due to a weaker phase synchronization between the supplementary motor cortex and left premotor and sensorimotor electrodes in patients. Thus, our findings support the hypothesis of a deficient phase coupling between the neuronal assemblies required to inhibit motor memory traces in patients with MD. EMG recorded from the right flexor pollicis longus muscle confirmed that patients with MD had a disrupted INH in NoGo trials. Hum Brain Mapp 2009.

Decrease in Early Right Alpha Band Phase Synchronization and Late Gamma Band Oscillations in Processing Syntax in Music

The present study investigated the neural correlates associated with the processing of music‐syntactical irregularities as compared with regular syntactic structures in music. Previous studies reported an early (∼200 ms) right anterior negative component (ERAN) by traditional event‐related‐potential analysis during music‐syntactical irregularities, yet little is known about the underlying oscillatory and synchronization properties of brain responses which are supposed to play a crucial role in general cognition including music perception. First we showed that the ERAN was primarily represented by low frequency (<8 Hz) brain oscillations. Further, we found that music‐syntactical irregularities as compared with music‐syntactical regularities, were associated with (i) an early decrease in the alpha band (9–10 Hz) phase synchronization between right fronto‐central and left temporal brain regions, and (ii) a late (∼500 ms) decrease in gamma band (38–50 Hz) oscillations over fronto‐central brain regions. These results indicate a weaker degree of long‐range integration when the musical expectancy is violated. In summary, our results reveal neural mechanisms of music‐syntactic processing that operate at different levels of cortical integration, ranging from early decrease in long‐range alpha phase synchronization to late local gamma oscillations. Hum Brain Mapp 2009.

Beta-band amplitude oscillations in the human internal globus pallidus support the encoding of sequence boundaries during initial sensorimotor sequence learning

Sequential behavior characterizes both simple everyday tasks, such as getting dressed, and complex skills, such as music performance. The basal ganglia (BG) play an important role in the learning of motor sequences. To study the contribution of the human BG to the initial encoding of sequence boundaries, we recorded local field potentials in the sensorimotor area of the internal globus pallidus (GPi) during the early acquisition of sensorimotor sequences in patients undergoing deep brain stimulation for dystonia. We demonstrated an anticipatory modulation of pallidal beta-band neuronal oscillations that was specific to sequence boundaries, as compared to within-sequence elements, and independent of both the movement parameters and the initiation/termination of ongoing movement. The modulation at sequence boundaries emerged with training, in parallel with skill learning, and correlated with the degree of long-range temporal correlations (LRTC) in the dynamics of ongoing beta-band amplitude oscillations. The implication is that LRTC of beta-band oscillations in the sensorimotor GPi might facilitate the emergence of beta power modulations by the sequence boundaries in parallel with sequence learning. Taken together, the results reveal the oscillatory mechanisms in the human BG that contribute at an initial learning phase to the hierarchical organization of sequential behavior as reflected in the formation of boundary-delimited representations of action sequences.

Involvement of Human Internal Globus Pallidus in the Early Modulation of Cortical Error-Related Activity

The detection and assessment of errors are a prerequisite to adapt behavior and improve future performance. Error monitoring is afforded by the interplay between cortical and subcortical neural systems. Ample evidence has pointed to a specific cortical error-related evoked potential, the error-related negativity (ERN), during the detection and evaluation of response errors. Recent models of reinforcement learning implicate the basal ganglia (BG) in early error detection following the learning of stimulus-response associations and in the modulation of the cortical ERN. To investigate the influence of the human BG motor output activity on the cortical ERN during response errors, we recorded local field potentials from the sensorimotor area of the internal globus pallidus and scalp electroencephalogram representing activity from the posterior medial frontal cortex in patients with idiopathic dystonia (hands not affected) during a flanker task. In error trials, a specific pallidal error-related potential arose 60 ms prior to the cortical ERN. The error-related changes in pallidal activity-characterized by theta oscillations-were predictive of the cortical error-related activity as assessed by Granger causality analysis. Our findings show an early modulation of error-related activity in the human pallidum, suggesting that pallidal output influences the cortex at an early stage of error detection.

Enhanced low-frequency oscillatory activity of the subthalamic nucleus in a patient with dystonia.

Local field potentials were recorded from the subthalamic nucleus (STN) in a patient with dystonia to further elucidate disease‐specific aspects of basal ganglia oscillatory activity.

Long-range correlation properties in timing of skilled piano performance: the influence of auditory feedback and deep brain stimulation

Unintentional timing deviations during musical performance can be conceived of as timing errors. However, recent research on humanizing computer-generated music has demonstrated that timing fluctuations that exhibit long-range temporal correlations (LRTC) are preferred by human listeners. This preference can be accounted for by the ubiquitous presence of LRTC in human tapping and rhythmic performances. Interestingly, the manifestation of LRTC in tapping behavior seems to be driven in a subject-specific manner by the LRTC properties of resting-state background cortical oscillatory activity. In this framework, the current study aimed to investigate whether propagation of timing deviations during the skilled, memorized piano performance (without metronome) of 17 professional pianists exhibits LRTC and whether the structure of the correlations is influenced by the presence or absence of auditory feedback. As an additional goal, we set out to investigate the influence of altering the dynamics along the cortico-basal-ganglia-thalamo-cortical network via deep brain stimulation (DBS) on the LRTC properties of musical performance. Specifically, we investigated temporal deviations during the skilled piano performance of a non-professional pianist who was treated with subthalamic-deep brain stimulation (STN-DBS) due to severe Parkinsons disease, with predominant tremor affecting his right upper extremity. In the tremor-affected right hand, the timing fluctuations of the performance exhibited random correlations with DBS OFF. By contrast, DBS restored long-range dependency in the temporal fluctuations, corresponding with the general motor improvement on DBS. Overall, the present investigations demonstrate the presence of LRTC in skilled piano performances, indicating that unintentional temporal deviations are correlated over a wide range of time scales. This phenomenon is stable after removal of the auditory feedback, but is altered by STN-DBS, which suggests that cortico-basal ganglia-thalamocortical circuits play a role in the modulation of the serial correlations of timing fluctuations exhibited in skilled musical performance.

Error monitoring is altered in musician's dystonia: evidence from ERP-based studies

Musicians dystonia (MD) is a task‐specific movement disorder characterized by a loss of voluntary motor control in highly trained movements like piano playing. Its underlying pathophysiology is defined by deficient functioning of neural pathways at different levels of the central nervous system. However, a few studies have examined the brain responses associated with executive functions such as error monitoring in MD. We recorded the electroencephalogram (EEG) in professional pianists during the performance of memorized music sequences at fast tempi. Event‐related potentials (ERPs) locked to pitch errors were investigated in MD and a control group. In MD patients, significantly larger error‐related brain responses before and following errors were observed as compared with healthy pianists. Our results suggest that in MD, the generalized degraded neural activity at all levels of the central nervous system is manifested in specific neural correlates of the executive functions that monitor an overlearned sensorimotor performance.