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137
Vocal experimentation in the juvenile songbird requires a basal ganglia circuit
, 2005
"... 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 ..."
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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. Citation: Ölveczky BP, Andalman AS, Fee MS (2005) Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol 3(5): e153. PLoS BIOLOGY
A Novel Reinforcement Model of Birdsong Vocalization Learning
- In
, 1995
"... Songbirds learn to imitate a tutor song through auditory and motor learning. We have developed a theoretical framework for song learning that accounts for response properties of neurons that have been observed in many of the nuclei that are involved in song learning. Specifically, we suggest that th ..."
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Songbirds learn to imitate a tutor song through auditory and motor learning. We have developed a theoretical framework for song learning that accounts for response properties of neurons that have been observed in many of the nuclei that are involved in song learning. Specifically, we suggest that the anterior forebrain pathway, which is not needed for song production in the adult but is essential for song acquisition, provides synaptic perturbations and adaptive evaluations for syllable vocalization learning. A computer model based on reinforcement learning was constructed that could replicate a real zebra finch song with 90% accuracy based on a spectrographic measure. The second generation of the birdsong model replicated the tutor song with 96% accuracy. 1 INTRODUCTION Studies of motor pattern generation have generally focussed on innate motor behaviors that are genetically preprogrammed and fine-tuned by adaptive mechanisms (Harris-Warrick et al., 1992). Birdsong learning provides ...
Birdbrains could teach basal ganglia research a new song. Trends Neurosci
, 2005
"... Recent advances in anatomical, physiological and histochemical characterization of avian basal ganglia neurons and circuitry have revealed remarkable similarities to mammalian basal ganglia. A modern revision of the avian anatomical nomenclature has now provided a common language for studying the fu ..."
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Recent advances in anatomical, physiological and histochemical characterization of avian basal ganglia neurons and circuitry have revealed remarkable similarities to mammalian basal ganglia. A modern revision of the avian anatomical nomenclature has now provided a common language for studying the function of the cortical–basal-ganglia–cortical loop, enabling neuroscientists to take advantage of the specialization of basal ganglia areas in various avian species. For instance, songbirds, which learn their vocal motor behavior using sensory feedback, have specialized a portion of their cortical–basal ganglia circuitry for song learning and production. This discrete circuit dedicated to a specific sensorimotor task could be especially tractable for elucidating the interwoven sensory, motor and reward signals carried by basal ganglia, and the function of these signals in task learning and execution.
Reinforcement learning with modulated spike timing-dependent synaptic plasticity
- Journal of Neurophysiology
, 2007
"... You might find this additional info useful... Supplementary material for this article can be found at: ..."
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You might find this additional info useful... Supplementary material for this article can be found at:
An associational model of birdsong sensorimotor learning. I. Efference copy and the learning of song syllables.
- J. Neurophysiol.
, 2000
"... Troyer, Todd W. and Allison J. Doupe. An associational model of birdsong sensorimotor learning. I. Efference copy and the learning of song syllables. J Neurophysiol 84: 1204 -1223, 2000. Birdsong learning provides an ideal model system for studying temporally complex motor behavior. Guided by the w ..."
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Cited by 21 (1 self)
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Troyer, Todd W. and Allison J. Doupe. An associational model of birdsong sensorimotor learning. I. Efference copy and the learning of song syllables. J Neurophysiol 84: 1204 -1223, 2000. Birdsong learning provides an ideal model system for studying temporally complex motor behavior. Guided by the well-characterized functional anatomy of the song system, we have constructed a computational model of the sensorimotor phase of song learning. Our model uses simple Hebbian and reinforcement learning rules and demonstrates the plausibility of a detailed set of hypotheses concerning sensory-motor interactions during song learning. The model focuses on the motor nuclei HVc and robust nucleus of the archistriatum (RA) of zebra finches and incorporates the long-standing hypothesis that a series of song nuclei, the Anterior Forebrain Pathway (AFP), plays an important role in comparing the bird's own vocalizations with a previously memorized song, or "template." This "AFP comparison hypothesis" is challenged by the significant delay that would be experienced by presumptive auditory feedback signals processed in the AFP. We propose that the AFP does not directly evaluate auditory feedback, but instead, receives an internally generated prediction of the feedback signal corresponding to each vocal gesture, or song "syllable." This prediction, or "efference copy," is learned in HVc by associating premotor activity in RA-projecting HVc neurons with the resulting auditory feedback registered within AFP-projecting HVc neurons. We also demonstrate how negative feedback "adaptation" can be used to separate sensory and motor signals within HVc. The model predicts that motor signals recorded in the AFP during singing carry sensory information and that the primary role for auditory feedback during song learning is to maintain an accurate efference copy. The simplicity of the model suggests that associational efference copy learning may be a common strategy for overcoming feedback delay during sensorimotor learning.
Development of intrinsic and synaptic properties in a forebrain nucleus essential to avian song learning
- J Neurosci
, 1997
"... In male zebra finches, the lateral magnocellular nucleus of the anterior neostriatum (LMAN) is necessary for the development of learned song but is not required for the production of acoustically stereotyped (crystallized) adult song. One hypothesis is that the physiological properties of LMAN neuro ..."
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In male zebra finches, the lateral magnocellular nucleus of the anterior neostriatum (LMAN) is necessary for the development of learned song but is not required for the production of acoustically stereotyped (crystallized) adult song. One hypothesis is that the physiological properties of LMAN neurons change over development and thus limit the ability of LMAN to affect song. To test this idea, we used in vitro intracellular recordings to characterize the intrinsic and synaptic properties of LMAN neurons in fledgling [posthatch days (PHD) 22–32] and juvenile zebra finches (PHD 40–51) when LMAN lesions disrupt normal song development, and in adults (�PHD 90) when LMAN lesions are without effect. In fledglings, depolarizing currents caused LMAN projection neurons to fire bursts of action potentials because of a putative low-threshold calcium spike (LTS). In contrast, juvenile and adult LMAN projection neurons
Molecular mapping of brain areas involved in parrot vocal communication
- J. Comp. Neurol
, 2000
"... Molecular mapping of brain areas involved in parrot vocal communication ..."
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Molecular mapping of brain areas involved in parrot vocal communication
Why are some neurons replaced in adult brain
- J. Neurosci
"... I will review recent observations on the production and replacement of neurons in the adult avian brain. I will highlight the fact that the new neurons are temporary, that they replace older ones that have died, and that the spontaneous replacement of neurons calls for a new theory of long-term memo ..."
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I will review recent observations on the production and replacement of neurons in the adult avian brain. I will highlight the fact that the new neurons are temporary, that they replace older ones that have died, and that the spontaneous replacement of neurons calls for a new theory of long-term memory. This theory is new only in relative terms, for it was first proposed 17 years ago (Nottebohm, 1984, 1985). Neurogenesis affects a minority of cell types in adult brain New neurons are added to many parts of the adult avian forebrain, but few, if any, are added elsewhere in the CNS of birds (Nottebohm, 1985). At least that has been the case under the conditions and in the species studied so far (mostly the canary Serinus canaria and zebra finch Taeniopygia guttata). Within the forebrain new neurons are added only to some, narrowly defined
Behavioral/Systems/Cognitive Auditory-Dependent Vocal Recovery in Adult Male Zebra Finches Is Facilitated by Lesion of a Forebrain Pathway That Includes the Basal Ganglia
"... The integration of two neural pathways generates learned song in zebra finches. The vocal motor pathway (VMP) is a direct connection between HVC (proper name) and the robust nucleus of the arcopallium (RA), whereas the anterior forebrain pathway (AFP) comprises an indirect circuit from HVC to RA tha ..."
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The integration of two neural pathways generates learned song in zebra finches. The vocal motor pathway (VMP) is a direct connection between HVC (proper name) and the robust nucleus of the arcopallium (RA), whereas the anterior forebrain pathway (AFP) comprises an indirect circuit from HVC to RA that traverses the basal ganglia. Partial ablation (microlesion) of HVC in adult birds alters the integration of VMP and AFP synaptic input within RA and destabilizes singing. However, the vocal pattern shows surprising resilience because birds subsequently recover their song in �1 week. Here, we show that deafening prevents vocal recovery after HVC microlesions, indicating that birds require auditory feedback to restore/relearn their vocal patterns. We then tested the role of the AFP (basal ganglia circuit) in this feedback-based recovery by ablating the output nucleus of the AFP [lateral magnocellular nucleus of the anterior nidopallium (LMAN)]. We found that LMAN ablation after HVC microlesions induced a sudden recovery of the vocal pattern. Thus, the AFP cannot be the neural locus of an instructive/learning mechanism that uses auditory feedback to guide vocal recovery, at least in this form of adult vocal plasticity. Instead, the AFP appears to be the source of the variable motor patterns responsible for vocal destabilization. In part, auditory feedback may restore song by strengthening the VMP component of synaptic input to RA relative to the AFP component. Key words: songbird; ablation; auditory feedback; vocal plasticity; sensorimotor; deafening
2005 The evolution of cerebrotypes in birds
- Brain Behav. Evol
"... Abstract Multivariate analyses of brain composition in mammals, amphibians and fish have revealed the evolution of 'cerebrotypes' that reflect specific niches and/or clades. Here, we present the first demonstration of similar cerebrotypes in birds. Using principal component analysis and h ..."
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Abstract Multivariate analyses of brain composition in mammals, amphibians and fish have revealed the evolution of 'cerebrotypes' that reflect specific niches and/or clades. Here, we present the first demonstration of similar cerebrotypes in birds. Using principal component analysis and hierarchical clustering methods to analyze a data set of 67 species, we demonstrate that five main cerebrotypes can be recognized. One type is dominated by galliforms and pigeons, among other species, that all share relatively large brainstems, but can be further differentiated by the proportional size of the cerebellum and telencephalic regions. The second cerebrotype contains a range of species that all share relatively large cerebellar and small nidopallial volumes. A third type is composed of two species, the tawny frogmouth (Podargus strigoides) and an owl, both of which share extremely large Wulst volumes. Parrots and passerines, the principal members of the fourth group, possess much larger nidopallial, mesopallial and striatopallidal proportions than the other groups. The fifth cerebrotype contains species such as raptors and waterfowl that are not found at the extremes for any of the brain regions and could therefore be classified as 'generalist' brains. Overall, the clustering of species does not directly reflect the phylogenetic relationships among species, but there is a tendency for species within an order to clump together. There may also be a weak relationship between cerebrotype and developmental differences, but two of the main clusters contained species with both altricial and precocial developmental patterns. As a whole, the groupings do agree with behavioral and ecological similarities among species. Most notably, species that share similarities in locomotor behavior, mode of prey capture or cognitive ability are clustered together. The relationship between cerebrotype and behavior/ecology in birds suggests that future comparative studies of brain-behavior relationships will benefit from adopting a multivariate approach.