Long-Term Potentiation in an Avian Basal Ganglia Nucleus Essential for Vocal Learning

Vocal learning in songbirds provides an excellent model for sensorimotor learning in vertebrates, with an accessible, well-defined behavior and discrete neural substrate. The rich behavioral plasticity exhibited by songbirds, however, contrasts starkly with the scarcity of candidate cellular mechanisms. Here, we report for the first time on an activity-dependent form of synaptic plasticity in area X, a component of the song system required for song learning and song maintenance. In slice preparations of zebra finch area X, pairing of high-frequency presynaptic stimulation with postsynaptic depolarization induces Hebbian long-term potentiation (LTP) of the glutamatergic inputs to spiny neurons. This form of LTP requires activation of NMDA receptors and D1-like dopamine receptors. In addition, LTP is observed in birds as young as 47 d after hatching and also in adult birds but not in younger birds, providing evidence of developmental regulation of the onset of synaptic plasticity. These properties make this form of LTP the best known candidate mechanism for reinforcement-based vocal learning in juveniles and song maintenance in adult birds.

[1]  P. Calabresi,et al.  Long‐term Potentiation in the Striatum is Unmasked by Removing the Voltage‐dependent Magnesium Block of NMDA Receptor Channels , 1992, The European journal of neuroscience.

[2]  A. Doupe,et al.  Singing-Related Neural Activity in a Dorsal Forebrain–Basal Ganglia Circuit of Adult Zebra Finches , 1999, The Journal of Neuroscience.

[3]  J. Bargas,et al.  D1 Receptor Activation Enhances Evoked Discharge in Neostriatal Medium Spiny Neurons by Modulating an L-Type Ca2+ Conductance , 1997, The Journal of Neuroscience.

[4]  R. Nicoll,et al.  The current excitement in long term potentiation , 1988, Neuron.

[5]  Charles J. Wilson,et al.  Spontaneous firing patterns of identified spiny neurons in the rat neostriatum , 1981, Brain Research.

[6]  Terrence J. Sejnowski,et al.  A Novel Reinforcement Model of Birdsong Vocalization Learning , 1994, NIPS.

[7]  Long Ding,et al.  Presynaptic Depression of Glutamatergic Synaptic Transmission by D1-Like Dopamine Receptor Activation in the Avian Basal Ganglia , 2003, The Journal of Neuroscience.

[8]  G. E. Vates,et al.  Feedback circuitry within a song-learning pathway. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[9]  R. Malenka,et al.  Simultaneous LTP of non-NMDA- and LTD of NMDA-receptor-mediated responses in the nucleus accumbens , 1994, Nature.

[10]  A. Doupe,et al.  Intrinsic and thalamic excitatory inputs onto songbird LMAN neurons differ in their pharmacological and temporal properties. , 1998, Journal of neurophysiology.

[11]  K. Immelmann Song development in the zebra finch and other estrildid finches , 1969 .

[12]  A. Doupe,et al.  Interruption of a basal ganglia–forebrain circuit prevents plasticity of learned vocalizations , 2000, Nature.

[13]  R. Tsien,et al.  Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices , 1990, Nature.

[14]  A. Arnold,et al.  Forebrain lesions disrupt development but not maintenance of song in passerine birds. , 1984, Science.

[15]  M. Farries,et al.  A Telencephalic Nucleus Essential for Song Learning Contains Neurons with Physiological Characteristics of Both Striatum and Globus Pallidus , 2002, The Journal of Neuroscience.

[16]  H. Williams,et al.  Changes in adult zebra finch song require a forebrain nucleus that is not necessary for song production. , 1999, Journal of neurobiology.

[17]  A. Arnold,et al.  Evidence for a catecholaminergic projection to area X in the zebra finch , 1981, The Journal of comparative neurology.

[18]  D. Lovinger,et al.  Postsynaptic endocannabinoid release is critical to long-term depression in the striatum , 2002, Nature Neuroscience.

[19]  F. H. Lopes da Silva,et al.  Synaptic Plasticity in an In Vitro Slice Preparation of the Rat Nucleus Accumbens , 1993, The European journal of neuroscience.

[20]  R. Mooney,et al.  Development of Intrinsic and Synaptic Properties in a Forebrain Nucleus Essential to Avian Song Learning , 1997, The Journal of Neuroscience.

[21]  E. Nordeen,et al.  Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. , 1990, Behavioral and neural biology.

[22]  P. Greengard,et al.  Dopamine and cAMP-Regulated Phosphoprotein 32 kDa Controls Both Striatal Long-Term Depression and Long-Term Potentiation, Opposing Forms of Synaptic Plasticity , 2000, The Journal of Neuroscience.

[23]  F. Nottebohm,et al.  Central control of song in the canary, Serinus canarius , 1976, The Journal of comparative neurology.

[24]  T. Matsushima,et al.  D1-receptor dependent synaptic potentiation in the basal ganglia of quail chicks , 2001, Neuroreport.

[25]  Michael S. Brainard,et al.  Auditory feedback in learning and maintenance of vocal behaviour , 2000, Nature Reviews Neuroscience.

[26]  Charlotte A. Boettiger,et al.  Developmentally Restricted Synaptic Plasticity in a Songbird Nucleus Required for Song Learning , 2001, Neuron.

[27]  J. Wickens,et al.  Dopamine reverses the depression of rat corticostriatal synapses which normally follows high-frequency stimulation of cortex In vitro , 1996, Neuroscience.

[28]  Toru Shimizu,et al.  Development of the catecholaminergic innervation of the song system of the male zebra finch. , 1996, Journal of neurobiology.

[29]  Long Ding,et al.  Dopamine Modulates Excitability of Spiny Neurons in the Avian Basal Ganglia , 2002, The Journal of Neuroscience.

[30]  Gerald E. Hough,et al.  Revised nomenclature for avian telencephalon and some related brainstem nuclei , 2004, The Journal of comparative neurology.

[31]  P. Calabresi,et al.  Unilateral dopamine denervation blocks corticostriatal LTP. , 1999, Journal of neurophysiology.

[32]  F. Nottebohm,et al.  Age at Deafening Affects the Stability of Learned Song in Adult Male Zebra Finches , 2000, The Journal of Neuroscience.

[33]  S. Bottjer,et al.  Circuits, hormones, and learning: vocal behavior in songbirds. , 1997, Journal of neurobiology.

[34]  M S Brainard,et al.  Postlearning Consolidation of Birdsong: Stabilizing Effects of Age and Anterior Forebrain Lesions , 2001, The Journal of Neuroscience.

[35]  A. Reiner,et al.  Structural and functional evolution of the basal ganglia in vertebrates , 1998, Brain Research Reviews.

[36]  Charles J. Wilson,et al.  The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  G. Ball,et al.  Long‐term potentiation in the avian hippocampus does not require activation of the N‐methyl‐D‐aspartate (NMDA) receptor , 1993, Synapse.

[38]  Minmin Luo,et al.  An Avian Basal Ganglia Pathway Essential for Vocal Learning Forms a Closed Topographic Loop , 2001, The Journal of Neuroscience.

[39]  R. Nicoll,et al.  The role of Ca2+ entry via synaptically activated NMDA receptors in the induction of long-term potentiation , 1993, Neuron.

[40]  R. Mooney,et al.  Intrinsic and Extrinsic Contributions to Auditory Selectivity in a Song Nucleus Critical for Vocal Plasticity , 2000, The Journal of Neuroscience.

[41]  E. Stern,et al.  Physiology and Morphology of Intratelencephalically Projecting Corticostriatal-Type Neurons in Pigeons as Revealed by Intracellular Recording and Cell Filling , 2001, Brain, Behavior and Evolution.

[42]  P. Sah,et al.  Long-Term Potentiation of Synaptic Transmission in the Avian Hippocampus , 1998, Journal of Neuroscience.

[43]  B. Katz,et al.  Quantal components of the end‐plate potential , 1954, The Journal of physiology.

[44]  C. Harding,et al.  Changes in catecholamine levels and turnover rates in hypothalamic, vocal control, and auditory nuclei in male zebra finches during development. , 1998, Journal of neurobiology.

[45]  Sarah M. N. Woolley,et al.  Bengalese Finches Lonchura Striata Domestica Depend upon Auditory Feedback for the Maintenance of Adult Song , 1997, The Journal of Neuroscience.

[46]  J. Wickens,et al.  Dopamine D-1/D-5 receptor activation is required for long-term potentiation in the rat neostriatum in vitro. , 2001, Journal of neurophysiology.

[47]  G. Collingridge,et al.  Excitatory amino acids in synaptic transmission in the Schaffer collateral‐commissural pathway of the rat hippocampus. , 1983, The Journal of physiology.

[48]  W. Schultz Getting Formal with Dopamine and Reward , 2002, Neuron.

[49]  E. Nordeen,et al.  Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. , 1992, Behavioral and neural biology.

[50]  P. Calabresi,et al.  Abnormal Synaptic Plasticity in the Striatum of Mice Lacking Dopamine D2 Receptors , 1997, The Journal of Neuroscience.

[51]  R. Nicoll,et al.  Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. , 1993, Journal of neurophysiology.

[52]  M. Memo,et al.  Pharmacology and biochemistry of dopamine receptors in the central nervous system and peripheral tissue. , 1986, Journal of neural transmission. Supplementum.

[53]  R. Mooney Different Subthreshold Mechanisms Underlie Song Selectivity in Identified HVc Neurons of the Zebra Finch , 2000, The Journal of Neuroscience.

[54]  F. Nottebohm,et al.  A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  Masakazu Konishi,et al.  Decrystallization of adult birdsong by perturbation of auditory feedback , 1999, Nature.