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Neuroscience Graduate Program at UCSF
The Neural Basis of Vocal Learning in Songbirds
Our laboratory is interested in how the nervous system mediates behavior, especially complex behaviors that must be learned. Birdsong provides a very useful model system for the study of these issues, with particular parallels to human speech learning. Song is an intricate motor act that is learned by young birds in two distinct phases, both of which depends on the animal's auditory experience: first the bird memorizes a tutor song (sensory learning); later, the bird begins to sing, and, in a manner analogous to the acquisition of speech by human infants, uses auditory feedback to refine and correct its vocalizations until it produces an approximate match of the memorized tutor song (sensorimotor learning). There are critical periods for sensory learning of song, just as there are for some types of human learning. Moreover, a discrete set of brain areas, called the song system, controls song learning and production. Both the song system and the adult song behavior are sexually dimorphic, and are regulated by sex steroids. Finally, song learning and singing are highly social behaviors, and are modulated by social cues. All of these features give birdsong the potential to shed light on the neural basis of learning, and on factors which control and limit learning.
At present the laboratory is focused on several issues. For one, we are interested in a particular song circuit, the anterior forebrain pathway (AFP). Numerous behavioral studies have suggested that this specialized basal ganglia circuit plays an essential role in song learning. Using a variety of physiological, behavioral, anatomical, and theoretical techniques, we are studying how the different features of song are represented in this network, how the animal's auditory experience and vocal learning shape its neuronal properties, and what the crucial function of this pathway might be.
In electrophysiological studies in anesthetized juvenile birds, we have shown that the neurons in this pathway respond to a variety of sounds. As the bird learns its song, however, these same neurons become highly selective: they respond robustly to the sound of the bird's own song, and weakly or not at all to very similar songs of conspecific individuals or even to the bird's own song played in reverse. The temporally and acoustically complex auditory response properties of these neurons suggest that they encode a neural representation of song, formed and perhaps used during learning. Systematic manipulations of the stimulus, the bird's own song, have allowed us to analyze the response properties of these very selective neurons in a quantitative manner. Behavioral manipulations have also been useful: altering the the bird's vocal organ before onset of singing, so that the bird can never produce a good copy of the tutor song that it memorized, has demonstrated that both the tutor and the bird's own song are important for shaping the properties of these neurons. These cells may in fact be involved in comparing these two stimuli during the process of learning.
Since the bird normally hears its own song only during singing, we have also begun recording from this pathway in awake, behaving birds. This has demonstrated that AFP neurons are also highly active when the bird sings, and carry signals related to the motor act of singing as well as auditory responses. Behavioral experiments, using lesions of this pathway, suggest that these neurons may be required any time the bird changes its song, even in adulthood, and may encode an error signal when auditory feedback does not match the intended vocal output. Moreover, the activity of these neurons is dramatically affected by different social settings (singing alone vs. singing to a companion), raising the possibility that this circuit may also be involved in social modulation of singing and song learning.
Ongoing experiments include i) recording simultaneously from the AFP and its target song motor nucleus, in awake and anesthetized birds at various stages of learning, to understand how this circuit interacts with and affects the motor pathway; ii)in vitro brain slice studies of the AFP to assess the synaptic changes underlying song learning; and iii) tracking down the source of the social modulation of activity in this pathway, which we hypothesize to be dopamine, as well as how the altered activity affects behavior.
A second and new, although related, area of interest is the auditory pathway afferent to the song system (the Field L complex), which must ultimately contain neurons contributing both to song selectivity and tutor song template memorization, and might also be the source of innate predispositions of birds to learn only the songs of their own species. We are analyzing auditory neurons at different stages of Field L using complex song stimuli and quantitative analysis of receptive field properties. Ongoing projects include i) mapping of sequential auditory stations in Field L using the bird's own song and conspecific stimuli, and ii) investigating Field L responses to songs of the bird's own species and well as selected heterospecific songs, in both adult and juvenile birds, and iii) assessing the effects of early experience on auditory tuning in these auditory stations.See above
Adria Arteseros
Research Associate
B.S., California Polytechnic State University
Behavioral and anatomical studies of the song system
Laurie Stepanek
Postdoctoral Fellow
Ph.D., University of Miami
Brian Wright
Postdoctoral Fellow
University of Florida
Discovering features of natural stimuli relevant to forebrain auditory neurons
Eva Ihle
Postdoctoral Fellow
M.D., Ph.D., University of Chicago
Measuring & manipulating neurotransmission in the zebra finch basal ganglia
Gabriela Carrillo
Senior Research Associate
M.S., San Francisco State University
Role of dopamine in song learning and production
Kathy Nagel
Graduate Student
B.S., University of Chicago
Analysis of forebrain auditory circuits for song perception and recognition
Mimi Kao
Graduate Student
B.S. Stanford University
Interaction of a basal ganglia circuit for learning with motor areas for song
Sarah Woolley
Postdoctoral Fellow
Ph.D., University of Texas
Dopaminergic and social modulation of neural activity
Satoshi Kojima
Postdoctoral Fellow
Ph.D., Hokkaido University in Japan
Neural and behavioral analysis of vocal learning
Stephanie Palmer
Postdoctoral Fellow
Ph.D., University of Oxford
Synaptic mechanisms involved in song learning
Gunsoo Kim
Postdoctoral Fellow
Ph.D. University of Pittsburgh
Solis, M.M. and Doupe, A.J. (2000) Compromised neural selectivity for song in birds with impaired sensorimotor learning. Neuron. 25:109-121
Brainard, M.S. and Doupe, A. J. (2000) Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature. 404:762-766
Theunissen, F.E., Sen, K., and Doupe, A.J. (2000) Spectral-temporal receptive fields of nonlinear auditory neurons obtained using natural sounds. J Neurosci. 20(6):2315-2331
Troyer, T.W. and Doupe, A.J. (2000) An associational model of birdsong sensorimotor learning. I. Efference copy and the learning of song syllables. J Neurophys 84, 1204-23.
Troyer, T.W. and Doupe, A.J. (2000) An associational model of birdsong sensorimotor learning. II. Temporal hierarchies and the learning of song sequence. J Neurophys 84, 1224-39.
Brainard, M.S. and Doupe, A. J. (2001) Post-learning consolidation of birdsong: Stabilizing effects of age and anterior forebrain lesions. J Neurosci. 21:2501-2517.
Sen, K., Theunissen, F.E., and Doupe, A.J. (2001) Feature analysis of natural sounds in the songbird auditory forebrain. J Neurophys. 86:1445-1458
Boettiger, C.A. and Doupe, A.J. (2001) Developmentally restricted synaptic plasticity in a songbird nucleus required for song learning. Neuron. 31:809-818
Kimpo, R.R., Theunissen, F.E., and A.J. Doupe (2003) Propagation of correlated activity through multiple stages of a neural circuit. J Neurosci. 23 (13):5750-5761
Carrillo, G.D. and Doupe, A.J. (2004) Is the songbird area X striatal, pallidal, or both? An anatomical study. J. Comp Neurol. 473: 415-437Allison Doupe, M.D./Ph.D.
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