Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 27 September 1996:
Vol. 273. no. 5283, pp. 1871 - 1875
DOI: 10.1126/science.273.5283.1871
Prev | Table of Contents | Next

Reports

Temporal Hierarchical Control of Singing in Birds

Albert C. Yu and Daniel Margoliash *

Songs of birds comprise hierarchical sets of vocal gestures. In zebra finches, songs include notes and syllables (groups of notes) delivered in fixed sequences. During singing, premotor neurons in the forebrain nucleus HVc exhibited reliable changes in activity rates whose patterns were uniquely associated with syllable identity. Neurons in the forebrain nucleus robustus archistriatalis, which receives input from the HVc, exhibited precisely timed and structured bursts of activity that were uniquely associated with note identity. Hence, units of vocal behavior are represented hierarchically in the avian forebrain. The representation of temporal sequences at each level of the hierarchy may be established by means of a decoding process involving interactions of higher level input with intrinsic local circuitry. Behavior is apparently represented by precise temporal patterning of spike trains at lower levels of the hierarchy.

A. C. Yu, Committee on Neurobiology, University of Chicago, Chicago, IL 60637, USA.
D. Margoliash, Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637, USA.
*   To whom correspondence should be addressed.

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Plastic and Stable Electrophysiological Properties of Adult Avian Forebrain Song-Control Neurons across Changing Breeding Conditions.
J. Meitzen, A. L. Weaver, E. A. Brenowitz, and D. J. Perkel (2009)
J. Neurosci. 29, 6558-6567
   Abstract »    Full Text »    PDF »
Top-Down Regulation of Plasticity in the Birdsong System: "Premotor" Activity in the Nucleus HVC Predicts Song Variability Better Than It Predicts Song Features.
N. F. Day, A. K. Kinnischtzke, M. Adam, and T. A. Nick (2008)
J Neurophysiol 100, 2956-2965
   Abstract »    Full Text »    PDF »
Online Contributions of Auditory Feedback to Neural Activity in Avian Song Control Circuitry.
J. T. Sakata and M. S. Brainard (2008)
J. Neurosci. 28, 11378-11390
   Abstract »    Full Text »    PDF »
Central Contributions to Acoustic Variation in Birdsong.
S. J. Sober, M. J. Wohlgemuth, and M. S. Brainard (2008)
J. Neurosci. 28, 10370-10379
   Abstract »    Full Text »    PDF »
Spikes and Bursts in Two Types of Thalamic Projection Neurons Differentially Shape Sleep Patterns and Auditory Responses in a Songbird.
R. H. R. Hahnloser, C. Z.-H. Wang, A. Nager, and K. Naie (2008)
J. Neurosci. 28, 5040-5052
   Abstract »    Full Text »    PDF »
A Specialized Forebrain Circuit for Vocal Babbling in the Juvenile Songbird.
D. Aronov, A. S. Andalman, and M. S. Fee (2008)
Science 320, 630-634
   Abstract »    Full Text »    PDF »
A Linkage Map of the Zebra Finch Taeniopygia guttata Provides New Insights Into Avian Genome Evolution.
J. Stapley, T. R. Birkhead, T. Burke, and J. Slate (2008)
Genetics 179, 651-667
   Abstract »    Full Text »    PDF »
Social Modulation of Sequence and Syllable Variability in Adult Birdsong.
J. T. Sakata, C. M. Hampton, and M. S. Brainard (2008)
J Neurophysiol 99, 1700-1711
   Abstract »    Full Text »    PDF »
Telencephalic Neurons Monosynaptically Link Brainstem and Forebrain Premotor Networks Necessary for Song.
T. F. Roberts, M. E. Klein, M. F. Kubke, J. M. Wild, and R. Mooney (2008)
J. Neurosci. 28, 3479-3489
   Abstract »    Full Text »    PDF »
Bottom-Up Activation of the Vocal Motor Forebrain by the Respiratory Brainstem.
R. C. Ashmore, J. A. Renk, and M. F. Schmidt (2008)
J. Neurosci. 28, 2613-2623
   Abstract »    Full Text »    PDF »
Hemispheric Coordination Is Necessary for Song Production in Adult Birds: Implications for a Dual Role for Forebrain Nuclei in Vocal Motor Control.
R. C. Ashmore, M. Bourjaily, and M. F. Schmidt (2008)
J Neurophysiol 99, 373-385
   Abstract »    Full Text »    PDF »
Auditory-Dependent Vocal Recovery in Adult Male Zebra Finches Is Facilitated by Lesion of a Forebrain Pathway That Includes the Basal Ganglia.
J. A. Thompson, W. Wu, R. Bertram, and F. Johnson (2007)
J. Neurosci. 27, 12308-12320
   Abstract »    Full Text »    PDF »
Functional Connectivity Between Auditory Areas Field L and CLM and Song System Nucleus HVC in Anesthetized Zebra Finches.
S. S. Shaevitz and F. E. Theunissen (2007)
J Neurophysiol 98, 2747-2764
   Abstract »    Full Text »    PDF »
Steroid Hormones Act Transsynaptically within the Forebrain to Regulate Neuronal Phenotype and Song Stereotypy.
J. Meitzen, I. T. Moore, K. Lent, E. A. Brenowitz, and D. J. Perkel (2007)
J. Neurosci. 27, 12045-12057
   Abstract »    Full Text »    PDF »
Behavioral Measurements of a Temporally Precise Motor Code for Birdsong.
C. M. Glaze and T. W. Troyer (2007)
J. Neurosci. 27, 7631-7639
   Abstract »    Full Text »    PDF »
Singing-Related Activity of Identified HVC Neurons in the Zebra Finch.
A. A. Kozhevnikov and M. S. Fee (2007)
J Neurophysiol 97, 4271-4283
   Abstract »    Full Text »    PDF »
Template-Based Spike Pattern Identification With Linear Convolution and Dynamic Time Warping.
Z. Chi, W. Wu, Z. Haga, N. G. Hatsopoulos, and D. Margoliash (2007)
J Neurophysiol 97, 1221-1235
   Abstract »    Full Text »    PDF »
Sleep-Related Spike Bursts in HVC Are Driven by the Nucleus Interface of the Nidopallium.
R. H. R. Hahnloser and M. S. Fee (2007)
J Neurophysiol 97, 423-435
   Abstract »    Full Text »    PDF »
Widespread Capacity for Steroid Synthesis in the Avian Brain and Song System.
S. E. London, D. A. Monks, J. Wade, and B. A. Schlinger (2006)
Endocrinology 147, 5975-5987
   Abstract »    Full Text »    PDF »
A Behavioral Role for Feature Detection by Sensory Bursts.
G. Marsat and G. S. Pollack (2006)
J. Neurosci. 26, 10542-10547
   Abstract »    Full Text »    PDF »
Real-time contributions of auditory feedback to avian vocal motor control..
J. T. Sakata and M. S. Brainard (2006)
J. Neurosci. 26, 9619-9628
   Abstract »    Full Text »    PDF »
High Levels of New Neuron Addition Persist When the Sensitive Period for Song Learning Is Experimentally Prolonged.
L. Wilbrecht, H. Williams, N. Gangadhar, and F. Nottebohm (2006)
J. Neurosci. 26, 9135-9141
   Abstract »    Full Text »    PDF »
Lesions of an Avian Basal Ganglia Circuit Prevent Context-Dependent Changes to Song Variability.
M. H. Kao and M. S. Brainard (2006)
J Neurophysiol 96, 1441-1455
   Abstract »    Full Text »    PDF »
Sleep-Related Neural Activity in a Premotor and a Basal-Ganglia Pathway of the Songbird.
R. H. R. Hahnloser, A. A. Kozhevnikov, and M. S. Fee (2006)
J Neurophysiol 96, 794-812
   Abstract »    Full Text »    PDF »
Midbrain Periaqueductal Gray and Vocal Patterning in a Teleost Fish.
J. M. Kittelberger, B. R. Land, and A. H. Bass (2006)
J Neurophysiol 96, 71-85
   Abstract »    Full Text »    PDF »
Noradrenergic Modulation of Activity in a Vocal Control Nucleus In Vitro.
M. M. Solis and D. J. Perkel (2006)
J Neurophysiol 95, 2265-2276
   Abstract »    Full Text »    PDF »
Synaptic Interactions Underlying Song-Selectivity in the Avian Nucleus HVC Revealed by Dual Intracellular Recordings.
M. J. Rosen and R. Mooney (2006)
J Neurophysiol 95, 1158-1175
   Abstract »    Full Text »    PDF »
Temporal Structure in Zebra Finch Song: Implications for Motor Coding.
C. M. Glaze and T. W. Troyer (2006)
J. Neurosci. 26, 991-1005
   Abstract »    Full Text »    PDF »
Dynamic-Clamp Analysis of the Effects of Convergence on Spike Timing. II. Few Synaptic Inputs.
M. A. Xu-Friedman and W. G. Regehr (2005)
J Neurophysiol 94, 2526-2534
   Abstract »    Full Text »    PDF »
Physiology of Neuronal Subtypes in the Respiratory-Vocal Integration Nucleus Retroamigualis of the Male Zebra Finch.
M. F. Kubke, Y. Yazaki-Sugiyama, R. Mooney, and J. M. Wild (2005)
J Neurophysiol 94, 2379-2390
   Abstract »    Full Text »    PDF »
Brainstem and Forebrain Contributions to the Generation of Learned Motor Behaviors for Song.
R. C. Ashmore, J. M. Wild, and M. F. Schmidt (2005)
J. Neurosci. 25, 8543-8554
   Abstract »    Full Text »    PDF »
Variable rate of singing and variable song duration are associated with high immediate early gene expression in two anterior forebrain song nuclei.
W.-c. Liu and F. Nottebohm (2005)
PNAS 102, 10724-10729
   Abstract »    Full Text »    PDF »
Selectivity of Canary HVC Neurons for the Bird's Own Song: Modulation by Photoperiodic Conditions.
C. Del Negro, K. Lehongre, and J.-M. Edeline (2005)
J. Neurosci. 25, 4952-4963
   Abstract »    Full Text »    PDF »
Freedom and Rules: The Acquisition and Reprogramming of a Bird's Learned Song.
T. J. Gardner, F. Naef, and F. Nottebohm (2005)
Science 308, 1046-1049
   Abstract »    Full Text »    PDF »
Sensorimotor Nucleus NIf Is Necessary for Auditory Processing But Not Vocal Motor Output in the Avian Song System.
J. A. Cardin, J. N. Raksin, and M. F. Schmidt (2005)
J Neurophysiol 93, 2157-2166
   Abstract »    Full Text »    PDF »
Rhythmic Activity in a Forebrain Vocal Control Nucleus In Vitro.
M. M. Solis and D. J. Perkel (2005)
J. Neurosci. 25, 2811-2822
   Abstract »    Full Text »    PDF »
Ensemble Coding of Vocal Control in Birdsong.
A. Leonardo and M. S. Fee (2005)
J. Neurosci. 25, 652-661
   Abstract »    Full Text »    PDF »
Mapping Neural Architectures Onto Acoustic Features of Birdsong.
H. D. I. Abarbanel, L. Gibb, G. B. Mindlin, and S. Talathi (2004)
J Neurophysiol 92, 96-110
   Abstract »    Full Text »    PDF »
Functional Specialization of Male and Female Vocal Motoneurons.
A. Yamaguchi, L. K. Kaczmarek, and D. B. Kelley (2003)
J. Neurosci. 23, 11568-11576
   Abstract »    Full Text »    PDF »
Pattern of Interhemispheric Synchronization in HVc During Singing Correlates With Key Transitions in the Song Pattern.
M. F. Schmidt (2003)
J Neurophysiol 90, 3931-3949
   Abstract »    Full Text »    PDF »
Long Memory in Song Learning by Zebra Finches.
Y. Funabiki and M. Konishi (2003)
J. Neurosci. 23, 6928-6935
   Abstract »    Full Text »    PDF »
State and Neuronal Class-Dependent Reconfiguration in the Avian Song System.
P. L. Rauske, S. D. Shea, and D. Margoliash (2003)
J Neurophysiol 89, 1688-1701
   Abstract »    Full Text »    PDF »
Respiratory and Telencephalic Modulation of Vocal Motor Neurons in the Zebra Finch.
C. B. Sturdy, J. M. Wild, and R. Mooney (2003)
J. Neurosci. 23, 1072-1086
   Abstract »    Full Text »    PDF »
Short-Term and Long-Term Effects of Vocal Distortion on Song Maintenance in Zebra Finches.
G. E. Hough II and S. F. Volman (2002)
J. Neurosci. 22, 1177-1186
   Abstract »    Full Text »    PDF »
Auditory representation of the vocal repertoire in a songbird with multiple song types.
R. Mooney, W. Hoese, and S. Nowicki (2001)
PNAS 98, 12778-12783
   Abstract »    Full Text »    PDF »
Postlearning Consolidation of Birdsong: Stabilizing Effects of Age and Anterior Forebrain Lesions.
M. S. Brainard and A. J. Doupe (2001)
J. Neurosci. 21, 2501-2517
   Abstract »    Full Text »    PDF »
Song Replay During Sleep and Computational Rules for Sensorimotor Vocal Learning.
A. S. Dave and D. Margoliash (2000)
Science 290, 812-816
   Abstract »    Full Text »
Song selectivity and sensorimotor signals in vocal learning and production.
M. M. Solis, M. S. Brainard, N. A. Hessler, and A. J. Doupe (2000)
PNAS 97, 11836-11842
   Abstract »    Full Text »    PDF »
An Associational Model of Birdsong Sensorimotor Learning I. Efference Copy and the Learning of Song Syllables.
T. W. Troyer and A. J. Doupe (2000)
J Neurophysiol 84, 1204-1223
   Abstract »    Full Text »    PDF »
An Associational Model of Birdsong Sensorimotor Learning II. Temporal Hierarchies and the Learning of Song Sequence.
T. W. Troyer and A. J. Doupe (2000)
J Neurophysiol 84, 1224-1239
   Abstract »    Full Text »    PDF »
Different Subthreshold Mechanisms Underlie Song Selectivity in Identified HVc Neurons of the Zebra Finch.
R. Mooney (2000)
J. Neurosci. 20, 5420-5436
   Abstract »    Full Text »    PDF »
Intrinsic and Extrinsic Contributions to Auditory Selectivity in a Song Nucleus Critical for Vocal Plasticity.
M. J. Rosen and R. Mooney (2000)
J. Neurosci. 20, 5437-5448
   Abstract »    Full Text »    PDF »
A relationship between behavior, neurotrophin expression, and new neuron survival.
X.-C. Li, E. D. Jarvis, B. Alvarez-Borda, D. A. Lim, and F. Nottebohm (2000)
PNAS
   Abstract »    Full Text »
Singing in the brain.
P. Marler and A. J. Doupe (2000)
PNAS 97, 2965-2967
   Full Text »    PDF »
Singing-Related Neural Activity in a Dorsal Forebrain-Basal Ganglia Circuit of Adult Zebra Finches.
N. A. Hessler and A. J. Doupe (1999)
J. Neurosci. 19, 10461-10481
   Abstract »    Full Text »    PDF »
Lesions of an Avian Forebrain Nucleus That Disrupt Song Development Alter Synaptic Connectivity and Transmission in the Vocal Premotor Pathway.
J. M. Kittelberger and R. Mooney (1999)
J. Neurosci. 19, 9385-9398
   Abstract »    Full Text »    PDF »
A GABAergic, Strongly Inhibitory Projection to a Thalamic Nucleus in the Zebra Finch Song System.
M. Luo and D. J. Perkel (1999)
J. Neurosci. 19, 6700-6711
   Abstract »    Full Text »    PDF »
Gradual Emergence of Song Selectivity in Sensorimotor Structures of the Male Zebra Finch Song System.
P. Janata and D. Margoliash (1999)
J. Neurosci. 19, 5108-5118
   Abstract »    Full Text »    PDF »
Long-Range Inhibition Within the Zebra Finch Song Nucleus RA Can Coordinate the Firing of Multiple Projection Neurons.
J. E. Spiro, M. B. Dalva, and R. Mooney (1999)
J Neurophysiol 81, 3007-3020
   Abstract »    Full Text »    PDF »
Interhemispheric Coordination of Premotor Neural Activity during Singing in Adult Zebra Finches.
E. T. Vu, M. F. Schmidt, and M. E. Mazurek (1998)
J. Neurosci. 18, 9088-9098
   Abstract »    Full Text »    PDF »
Multiple Cell Types Distinguished by Physiological, Pharmacological, and Anatomic Properties in Nucleus HVc of the Adult Zebra Finch.
P. Dutar, H. M. Vu, and D. J. Perkel (1998)
J Neurophysiol 80, 1828-1838
   Abstract »    Full Text »    PDF »
Electrophysiological Characteristics of Classes of Neuron in the HVc of the Zebra Finch.
M. Kubota and I. Taniguchi (1998)
J Neurophysiol 80, 914-923
   Abstract »    Full Text »    PDF »
Coding of Serial Order by Neostriatal Neurons: A "Natural Action" Approach to Movement Sequence.
J. W. Aldridge and K. C. Berridge (1998)
J. Neurosci. 18, 2777-2787
   Abstract »    Full Text »    PDF »
Slow Synaptic Inhibition in Nucleus HVc of the Adult Zebra Finch.
M. F. Schmidt and D. J. Perkel (1998)
J. Neurosci. 18, 895-904
   Abstract »    Full Text »    PDF »
Sex Difference in the Size of the Neural Song Control Regions in a Dueting Songbird with Similar Song Repertoire Size of Males and Females.
M. Gahr, E. Sonnenschein, and W. Wickler (1998)
J. Neurosci. 18, 1124-1131
   Abstract »    Full Text »    PDF »
Development of Intrinsic and Synaptic Properties in a Forebrain Nucleus Essential to Avian Song Learning.
F. S. Livingston and R. Mooney (1997)
J. Neurosci. 17, 8997-9009
   Abstract »    Full Text »    PDF »
Motor-driven gene expression.
E. D. Jarvis and F. Nottebohm (1997)
PNAS 94, 4097-4102
   Abstract »    Full Text »    PDF »
A relationship between behavior, neurotrophin expression, and new neuron survival.
X.-C. Li, E. D. Jarvis, B. Alvarez-Borda, D. A. Lim, and F. Nottebohm (2000)
PNAS 97, 8584-8589
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)