Virginia B. Penhune

Structure and function of auditory cortex: music and speech

We examine the evidence that speech and musical sounds exploit different acoustic cues: speech is highly dependent on rapidly changing broadband sounds, whereas tonal patterns tend to be slower, although small and precise changes in frequency are important. We argue that the auditory cortices in the two hemispheres are relatively specialized, such that temporal resolution is better in left auditory cortical areas and spectral resolution is better in right auditory cortical areas. We propose that cortical asymmetries might have developed as a general solution to the need to optimize processing of the acoustic environment in both temporal and frequency domains.

When the brain plays music: auditory-motor interactions in music perception and production.

Music performance is both a natural human activity, present in all societies, and one of the most complex and demanding cognitive challenges that the human mind can undertake. Unlike most other sensory–motor activities, music performance requires precise timing of several hierarchically organized actions, as well as precise control over pitch interval production, implemented through diverse effectors according to the instrument involved. We review the cognitive neuroscience literature of both motor and auditory domains, highlighting the value of studying interactions between these systems in a musical context, and propose some ideas concerning the role of the premotor cortex in integration of higher order features of music with appropriately timed and organized actions.

Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning

This review paper focuses on studies in healthy human subjects that examined the functional neuroanatomy and cerebral plasticity associated with the learning, consolidation and retention phases of motor skilled behaviors using modern brain imaging techniques. Evidence in support of a recent model proposed by Doyon and Ungerleider [Functional Anatomy of Motor Skill Learning. In: Squire LR, Schacter DL, editors. Neuropsychology of Memory. New York: Guilford Press, 2002.] is also discussed. The latter suggests that experience-dependent changes in the brain depend not only on the stage of learning, but also on whether subjects are required to learn a new sequence of movements (motor sequence learning) or learn to adapt to environmental perturbations (motor adaptation). This model proposes that the cortico-striatal and cortico-cerebellar systems contribute differentially to motor sequence learning and motor adaptation, respectively, and that this is most apparent during the slow learning phase (i.e. automatization) when subjects achieve asymptotic performance, as well as during reactivation of the new skilled behavior in the retention phase.

Contributions of the basal ganglia and functionally related brain structures to motor learning

This review discusses the cerebral plasticity, and the role of the cortico-striatal system in particular, observed as one is learning or planning to execute a newly learned motor behavior up to when the skill is consolidated or has become highly automatized. A special emphasis is given to imaging work describing the neural substrate mediating motor sequence learning and motor adaptation paradigms. These results are then put into a plausible neurobiological model of motor skill learning, which proposes an integrated view of the brain plasticity mediating this form of memory at different stages of the acquisition process.

Listening to Musical Rhythms Recruits Motor Regions of the Brain

Perception and actions can be tightly coupled; but does a perceptual event dissociated from action processes still engage the motor system? We conducted 2 functional magnetic resonance imaging studies involving rhythm perception and production to address this question. In experiment 1, on each trial subjects 1st listened in anticipation of tapping, and then tapped along with musical rhythms. Recruitment of the supplementary motor area, mid-premotor cortex (PMC), and cerebellum was observed during listen with anticipation. To test whether this activation was related to motor planning or rehearsal, in experiment 2 subjects naively listened to rhythms without foreknowledge that they would later tap along with them. Yet, the same motor regions were engaged despite no action-perception connection. In contrast, the ventral PMC was only recruited during action and action-coupled perceptual processes, whereas the dorsal part was only sensitive to the selection of actions based on higher-order rules of temporal organization. These functional dissociations shed light on the nature of action-perception processes and suggest an inherent link between auditory and motor systems in the context of rhythm.

Cerebellar Contributions to Motor Timing: A PET Study of Auditory and Visual Rhythm Reproduction

The perception and production of temporal patterns, or rhythms, is important for both music and speech. However, the way in which the human brain achieves accurate timing of perceptual input and motor output is as yet little understood. Central control of both motor timing and perceptual timing across modalities has been linked to both the cerebellum and the basal ganglia (BG). The present study was designed to test the hypothesized central control of temporal processing and to examine the roles of the cerebellum, BG, and sensory association areas. In this positron emission tomography (PET) activation paradigm, subjects reproduced rhythms of increasing temporal complexity that were presented separately in the auditory and visual modalities. The results provide support for a supramodal contribution of the lateral cerebellar cortex and cerebellar vermis to the production of a timed motor response, particularly when it is complex and/or novel. The results also give partial support to the involvement of BG structures in motor timing, although this may be more directly related to implementation of the motor response than to timing per se. Finally, sensory association areas and the ventrolateral frontal cortex were found to be involved in modality-specific encoding and retrieval of the temporal stimuli. Taken together, these results point to the participation of a number of neural structures in the production of a timed motor response from an external stimulus. The role of the cerebellum in timing is conceptualized not as a clock or counter but simply as the structure that provides the necessary circuitry for the sensory system to extract temporal information and for the motor system to learn to produce a precisely timed response.

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.

Interactions between auditory and dorsal premotor cortex during synchronization to musical rhythms

When listening to music, we often spontaneously synchronize our body movements to a rhythms beat (e.g. tapping our feet). The goals of this study were to determine how features of a rhythm such as metric structure, can facilitate motor responses, and to elucidate the neural correlates of these auditory-motor interactions using fMRI. Five variants of an isochronous rhythm were created by increasing the contrast in sound amplitude between accented and unaccented tones, progressively highlighting the rhythms metric structure. Subjects tapped in synchrony to these rhythms, and as metric saliency increased across the five levels, louder tones evoked longer tap durations with concomitant increases in the BOLD response at auditory and dorsal premotor cortices. The functional connectivity between these regions was also modulated by the stimulus manipulation. These results show that metric organization, as manipulated via intensity accentuation, modulates motor behavior and neural responses in auditory and dorsal premotor cortex. Auditory-motor interactions may take place at these regions with the dorsal premotor cortex interfacing sensory cues with temporally organized movement.

Parallel contributions of cerebellar, striatal and M1 mechanisms to motor sequence learning.

When learning a new motor sequence, we must execute the correct order of movements while simultaneously optimizing sensorimotor parameters such as trajectory, timing, velocity and force. Neurophysiological studies in animals and humans have identified the major brain regions involved in sequence learning, including the motor cortex (M1), basal ganglia (BG) and cerebellum. Current models link these regions to different stages of learning (early vs. late) or different components of performance (spatial vs. sensorimotor). At the same time, research in motor control has given rise to the concept that internal models at different levels of the motor system may contribute to learning. The goal of this review is to develop a new framework for motor sequence learning that combines stage and component models within the context of internal models. To do this, we review behavioral and neuroimaging studies in humans and neurophysiological studies in animals. Based on this evidence, we present a model proposing that sequence learning is underwritten by parallel, interacting processes, including internal model formation and sequence representation, that are instantiated in specific cerebellar, BG or M1 mechanisms depending on task demands and the stage of learning. The striatal system learns predictive stimulus-response associations and is critical for motor chunking. The role of the cerebellum is to acquire the optimal internal model for sequence performance in a particular context, and to contribute to error correction and control of on-going movement. M1 acts to store the representation of a learned sequence, likely as part of a distributed network including the parietal lobe and premotor cortex.

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.