Postdoctoral researcher, Tufts University
Boosting motor skill plasticity by altering activity in a cortical-basal ganglia brain circuit
Behavioral variability, or motor exploration, is critical for trial-and-error learning, including speech acquisition in humans and song learning in songbirds. In both these examples, vocalizations are learned by vocal practice early in life. In order to learn a good imitation of the adult template, both humans and songbirds use auditory feedback to match their vocalizations to a previously memorized model. Producing variable versions of vocalizations is important to achieve good learning.
In the avian brain, there is evidence that a region called ‘LMAN’ (lateral magnocellular nucleus of the anterior nidopallium) is the major site for generating neural variability that produces variability in song output. Inactivating LMAN reduces song variability and impairs song learning. LMAN is part of a cortical-basal ganglia circuit, which is a brain network that is critical for learning and performing motor skills and learning in response to reward. Cortical-basal ganglia circuits are highly conserved across vertebrates, and are a major site of motor pathology, such as in Parkinson’s or Huntington’s Disease.
In contrast to juveniles that sing variable songs that will improve over time and can learn to add new sounds to their song, adult zebra finches sing a very stable, stereotyped song. We are interested in investigating whether we can increase trial-to-trial variability in song in the service of learning. Moreover, we aim to harness this behavioral variability to increase the ability of adult birds to adaptively change their songs. Such studies have the potential to increase our understanding of how adult learning can be enhanced as well as inform therapies for basal ganglia motor disorders.
Abstract: Individual differences in motor learning ability are widely acknowledged, yet little is known about the factors that underlie them. Here we explore whether movement-to-movement variability in motor output, a ubiquitous if often unwanted characteristic of motor performance, predicts motor learning ability. Surprisingly, we found that higher levels of task-relevant motor variability predicted faster learning both across individuals and across tasks in two different paradigms, one relying on reward-based learning to shape specific arm movement trajectories and the other relying on error-based learning to adapt movements in novel physical environments. We proceeded to show that training can reshape the temporal structure of motor variability, aligning it with the trained task to improve learning. These results provide experimental support for the importance of action exploration, a key idea from reinforcement learning theory, showing that motor variability facilitates motor learning in humans and that our nervous systems actively regulate it to improve learning.
Pub.: 15 Jan '14, Pinned: 04 Jul '17
Abstract: Birdsong is considered a model of human speech development at behavioral and neural levels. Few direct tests of the proposed analogs exist, however. Here we test a mechanism of phonological development in human infants that is based on social shaping, a selective learning process first documented in songbirds. By manipulating mothers' reactions to their 8-month-old infants' vocalizations, we demonstrate that phonological features of babbling are sensitive to nonimitative social stimulation. Contingent, but not noncontingent, maternal behavior facilitates more complex and mature vocal behavior. Changes in vocalizations persist after the manipulation. The data show that human infants use social feedback, facilitating immediate transitions in vocal behavior. Social interaction creates rapid shifts to developmentally more advanced sounds. These transitions mirror the normal development of speech, supporting the predictions of the avian social shaping model. These data provide strong support for a parallel in function between vocal precursors of songbirds and infants. Because imitation is usually considered the mechanism for vocal learning in both taxa, the findings introduce social shaping as a general process underlying the development of speech and song.
Pub.: 17 Jun '03, Pinned: 03 Jul '17
Abstract: Human speech and birdsong have numerous parallels. Both humans and songbirds learn their complex vocalizations early in life, exhibiting a strong dependence on hearing the adults they will imitate, as well as themselves as they practice, and a waning of this dependence as they mature. Innate predispositions for perceiving and learning the correct sounds exist in both groups, although more evidence of innate descriptions of species-specific signals exists in songbirds, where numerous species of vocal learners have been compared. Humans also share with songbirds an early phase of learning that is primarily perceptual, which then serves to guide later vocal production. Both humans and songbirds have evolved a complex hierarchy of specialized forebrain areas in which motor and auditory centers interact closely, and which control the lower vocal motor areas also found in nonlearners. In both these vocal learners, however, how auditory feedback of self is processed in these brain areas is surprisingly unclear. Finally, humans and songbirds have similar critical periods for vocal learning, with a much greater ability to learn early in life. In both groups, the capacity for late vocal learning may be decreased by the act of learning itself, as well as by biological factors such as the hormones of puberty. Although some features of birdsong and speech are clearly not analogous, such as the capacity of language for meaning, abstraction, and flexible associations, there are striking similarities in how sensory experience is internalized and used to shape vocal outputs, and how learning is enhanced during a critical period of development. Similar neural mechanisms may therefore be involved.
Pub.: 15 Apr '99, Pinned: 03 Jul '17
Abstract: A hallmark of sensitive periods of development is an enhanced capacity for learning, such that experience exerts a profound effect on the brain resulting in the establishment of behaviors and underlying neural circuitry that can last a lifetime. Songbirds, like humans, have a sensitive period for vocal learning: they acquire the sounds used for vocal communication during a restricted period of development. In principle, any organism that undertakes vocal learning is faced with the same challenge: to form some representation of target vocal sounds based on auditory experience, and then to translate that auditory target into a motor program that reproduces the sound. Both birds and humans achieve this translation by using auditory (and other) feedback resulting from incipient vocalizations ("babbling" in humans, "subsong" in birds) to adjust motor commands until vocal output produces a good copy of the target sounds. Similarities between vocal learning in birds and humans suggest that many aspects of the learning process have evolved to meet demands imposed by vocal communication. Thus songbirds provide a valuable animal model in which to study the physiological basis of learned vocal communication and the nature of sensitive periods in general. In this article, I describe aspects of both behavioral and neural frameworks that currently inform our thinking about mechanisms underlying vocal learning and behavior in songbirds, and highlight ideas that may need re-examination.
Pub.: 18 Aug '04, Pinned: 03 Jul '17
Abstract: Songbirds, much like humans, learn their vocal behavior, and must be able to hear both themselves and others to do so. Studies of the brain areas involved in singing and song learning could reveal the underlying neural mechanisms. Here we describe experiments that explore the properties of the songbird anterior forebrain pathway (AFP), a basal ganglia-forebrain circuit known to be critical for song learning and for adult modification of vocal output. First, neural recordings in anesthetized, juvenile birds show that auditory AFP neurons become selectively responsive to the song stimuli that are compared during sensorimotor learning. Individual AFP neurons develop tuning to the bird's own song (BOS), and in many cases to the tutor song as well, even when these stimuli are manipulated to be very different from each other. Such dual selectivity could be useful in the BOS-tutor song comparison critical to song learning. Second, simultaneous neural recordings from the AFP and its target nucleus in the song motor pathway in anesthetized adult birds reveal correlated activity that is preserved through multiple steps of the circuits for song, including the AFP. This suggests that the AFP contains highly functionally interconnected neurons, an architecture that can preserve information about the timing of firing of groups of neurons. Finally, in vitro studies show that recurrent synapses between neurons in the AFP outflow nucleus, which are expected to contribute importantly to AFP correlation, can undergo activity-dependent and timing-sensitive strengthening. This synaptic enhancement appears to be restricted to birds in the sensory critical and early sensorimotor phases of learning. Together, these studies show that the AFP contains cells that reflect learning of both BOS and tutor song, as well as developmentally regulated synaptic and circuit mechanisms well-suited to create temporally organized assemblies of such cells. Such experience-dependent sensorimotor assemblies are likely to be critical to the AFP's role in song learning. Moreover, studies of such mechanisms in this basal ganglia circuit specialized for song may shed light more generally on how basal ganglia circuits function in guiding motor learning using sensory feedback signals.
Pub.: 18 Aug '04, Pinned: 03 Jul '17
Abstract: Most of our motor skills are not innately programmed, but are learned by a combination of motor exploration and performance evaluation, suggesting that they proceed through a reinforcement learning (RL) mechanism. Songbirds have emerged as a model system to study how a complex behavioral sequence can be learned through an RL-like strategy. Interestingly, like motor sequence learning in mammals, song learning in birds requires a basal ganglia (BG)-thalamocortical loop, suggesting common neural mechanisms. Here, we outline a specific working hypothesis for how BG-forebrain circuits could utilize an internally computed reinforcement signal to direct song learning. Our model includes a number of general concepts borrowed from the mammalian BG literature, including a dopaminergic reward prediction error and dopamine-mediated plasticity at corticostriatal synapses. We also invoke a number of conceptual advances arising from recent observations in the songbird. Specifically, there is evidence for a specialized cortical circuit that adds trial-to-trial variability to stereotyped cortical motor programs, and a role for the BG in "biasing" this variability to improve behavioral performance. This BG-dependent "premotor bias" may in turn guide plasticity in downstream cortical synapses to consolidate recently learned song changes. Given the similarity between mammalian and songbird BG-thalamocortical circuits, our model for the role of the BG in this process may have broader relevance to mammalian BG function.
Pub.: 22 Oct '11, Pinned: 03 Jul '17
Abstract: Songbirds learn their songs by trial-and-error experimentation, producing highly variable vocal output as juveniles. By comparing their own sounds to the song of a tutor, young songbirds gradually converge to a stable song that can be a remarkably good copy of the tutor song. Here we show that vocal variability in the learning songbird is induced by a basal-ganglia-related circuit, the output of which projects to the motor pathway via the lateral magnocellular nucleus of the nidopallium (LMAN). We found that pharmacological inactivation of LMAN dramatically reduced acoustic and sequence variability in the songs of juvenile zebra finches, doing so in a rapid and reversible manner. In addition, recordings from LMAN neurons projecting to the motor pathway revealed highly variable spiking activity across song renditions, showing that LMAN may act as a source of variability. Lastly, pharmacological blockade of synaptic inputs from LMAN to its target premotor area also reduced song variability. Our results establish that, in the juvenile songbird, the exploratory motor behavior required to learn a complex motor sequence is dependent on a dedicated neural circuit homologous to cortico-basal ganglia circuits in mammals.
Pub.: 14 Apr '05, Pinned: 30 Jun '17
Abstract: Trial-to-trial variability in the execution of movements and motor skills is ubiquitous and widely considered to be the unwanted consequence of a noisy nervous system. However, recent studies have suggested that motor variability may also be a feature of how sensorimotor systems operate and learn. This view, rooted in reinforcement learning theory, equates motor variability with purposeful exploration of motor space that, when coupled with reinforcement, can drive motor learning. Here we review studies that explore the relationship between motor variability and motor learning in both humans and animal models. We discuss neural circuit mechanisms that underlie the generation and regulation of motor variability and consider the implications that this work has for our understanding of motor learning. Expected final online publication date for the Annual Review of Neuroscience Volume 40 is July 8, 2017. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Pub.: 11 May '17, Pinned: 30 Jun '17
Abstract: Many motor behaviors, from walking to speaking, are acquired through experience, in particular, through trial-and-error learning. The acquisition and maintenance of such motor behaviors in a wide range of species, including humans, appear to depend on cortical-basal ganglia circuits. In this review, we discuss recent studies in songbirds that have been pivotal in informing our current understanding of motor learning and cortical-basal ganglia function. Songbirds are important ethological model systems for the study of motor learning because young songbirds naturally develop and refine their songs through trial-and-error learning. In addition, reinforcement mechanisms are hypothesized to be important for the maintenance and plasticity of structured adult song. Computational and experimental studies highlight the importance of vocal motor variability as the substrate upon which reinforcement mechanisms could operate to shape developing song and to maintain adult song. Recent studies in songbirds indicate that this vocal motor variability is actively generated and modulated by a highly specialized cortical-basal ganglia circuit evolved for a single behavior, song. We argue that these and other recent findings illustrate how the tight association between a specialized neural circuit and a natural behavior make songbirds a unique and powerful model in which to investigate the neural substrates of motor learning and plasticity.
Pub.: 03 Dec '14, Pinned: 30 Jun '17
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