Anatomy of a songbird basal ganglia circuit essential for vocal learning and plasticity

Vocal learning in songbirds requires an anatomically discrete and functionally dedicated circuit called the anterior forebrain pathway (AFP). The AFP is homologous to cortico-basal ganglia-thalamo-cortical loops in mammals. The basal ganglia portion of this pathway, Area X, shares many features characteristic of the mammalian striatum and pallidum, including cell types and connectivity. The AFP also deviates from mammalian basal ganglia circuits in fundamental ways. In addition, the microcircuitry, role of neuromodulators, and function of Area X are still unclear. Elucidating the mechanisms by which both mammalian-like and unique features of the AFP contribute to vocal learning may help lead to a broad understanding of the sensorimotor functions of basal ganglia circuits.

[1]  Edward A. Stern,et al.  Birdbrains could teach basal ganglia research a new song , 2005, Trends in Neurosciences.

[2]  L. Acsády,et al.  Structural Correlates of Efficient GABAergic Transmission in the Basal Ganglia–Thalamus Pathway , 2008, The Journal of Neuroscience.

[3]  Gregory F Ball,et al.  Photoperiod‐Dependent and ‐Independent Regulation of Melatonin Receptors in the Forebrain of Songbirds , 2000, Journal of neuroendocrinology.

[4]  R. Malenka,et al.  Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. , 2000, Annual review of neuroscience.

[5]  Gregory F Ball,et al.  A role for norepinephrine in the regulation of context‐dependent ZENK expression in male zebra finches (Taeniopygia guttata) , 2005, The European journal of neuroscience.

[6]  D. Perkel,et al.  Long‐range GABAergic projection in a circuit essential for vocal learning , 1999, The Journal of comparative neurology.

[7]  Fernando Nottebohm,et al.  Reafferent thalamo‐“cortical” loops in the song system of oscine songbirds , 1997, The Journal of comparative neurology.

[8]  Allison J. Doupe,et al.  Neurons in a Forebrain Nucleus Required for Vocal Plasticity Rapidly Switch between Precise Firing and Variable Bursting Depending on Social Context , 2008, The Journal of Neuroscience.

[9]  A. Graybiel Habits, rituals, and the evaluative brain. , 2008, Annual review of neuroscience.

[10]  A. Reiner,et al.  The efferent projections of the dorsal and ventral pallidal parts of the pigeon basal ganglia, studied with biotinylated dextran amine , 1997, Neuroscience.

[11]  A. Doupe Song- and Order-Selective Neurons in the Songbird Anterior Forebrain and their Emergence during Vocal Development , 1997, The Journal of Neuroscience.

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

[13]  Abigail L. Person,et al.  Unitary IPSPs Drive Precise Thalamic Spiking in a Circuit Required for Learning , 2005, Neuron.

[14]  J. Tepper,et al.  GABAergic control of substantia nigra dopaminergic neurons. , 2007, Progress in brain research.

[15]  Gregory F Ball,et al.  Characterization and localization of D1 dopamine receptors in the sexually dimorphic vocal control nucleus, area X, and the basal ganglia of European starlings. , 1994, Journal of neurobiology.

[16]  S. Bottjer,et al.  Sex differences in neuropeptide staining of song-control nuclei in zebra finch brains. , 1997, Brain, behavior and evolution.

[17]  J. Deniau,et al.  Disinhibition as a basic process in the expression of striatal functions , 1990, Trends in Neurosciences.

[18]  Y. Smith,et al.  The thalamostriatal system: a highly specific network of the basal ganglia circuitry , 2004, Trends in Neurosciences.

[19]  F. Johnson,et al.  Cannabinoid exposure alters learning of zebra finch vocal patterns. , 2003, Brain research. Developmental brain research.

[20]  W. Schultz Multiple dopamine functions at different time courses. , 2007, Annual review of neuroscience.

[21]  Aaron S. Andalman,et al.  Vocal Experimentation in the Juvenile Songbird Requires a Basal Ganglia Circuit , 2005, PLoS biology.

[22]  R. Llinás,et al.  Bursting of thalamic neurons and states of vigilance. , 2006, Journal of neurophysiology.

[23]  P. Kalivas,et al.  GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area , 1993, Neuroscience.

[24]  J. Storm-Mathisen,et al.  The Expression of Vesicular Glutamate Transporters Defines Two Classes of Excitatory Synapse , 2001, Neuron.

[25]  Anatol C. Kreitzer,et al.  Striatal Plasticity and Basal Ganglia Circuit Function , 2008, Neuron.

[26]  F. Horak,et al.  Influence of the globus pallidus on arm movements in monkeys. III. Timing of movement-related information. , 1985, Journal of neurophysiology.

[27]  N. Hessler,et al.  Role of the midbrain dopaminergic system in modulation of vocal brain activation by social context , 2007, The European journal of neuroscience.

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

[29]  J. Bolam,et al.  A Dopaminergic Axon Lattice in the Striatum and Its Relationship with Cortical and Thalamic Terminals , 2008, The Journal of Neuroscience.

[30]  A. Csillag,et al.  Connectivity of the lobus parolfactorius of the domestic chicken (Gallus domesticus): An anterograde and retrograde pathway tracing study , 1994, The Journal of comparative neurology.

[31]  A. Doupe,et al.  Activity Propagation in an Avian Basal Ganglia-Thalamocortical Circuit Essential for Vocal Learning , 2009, The Journal of Neuroscience.

[32]  H. Bergman,et al.  Lack of spike-count and spike-time correlations in the substantia nigra reticulata despite overlap of neural responses. , 2007, Journal of neurophysiology.

[33]  Max Kleiman-Weiner,et al.  Differential electrophysiological properties of dopamine D1 and D2 receptor‐containing striatal medium‐sized spiny neurons , 2008, The European journal of neuroscience.

[34]  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.

[35]  V. Cassone,et al.  Melatonin Binding in the House Sparrow Song Control System: Sexual Dimorphism and the Effect of Photoperiod , 1996, Hormones and Behavior.

[36]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. , 1983, Journal of neurophysiology.

[37]  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.

[38]  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.

[39]  A. Arnold,et al.  Enkephalin-like immunoreactivity in vocal control regions of the zebra finch brain , 1981, Brain Research.

[40]  R. Wurtz,et al.  Modification of saccadic eye movements by GABA-related substances. II. Effects of muscimol in monkey substantia nigra pars reticulata. , 1985, Journal of neurophysiology.

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

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

[43]  G. Bentley Melatonin receptor density in Area X of European starlings is correlated with reproductive state and is unaffected by plasma melatonin concentration. , 2003, General and comparative endocrinology.

[44]  H. Kita,et al.  Excitatory Cortical Inputs to Pallidal Neurons Via the Subthalamic Nucleus in the Monkey , 2000 .

[45]  A. Doupe,et al.  Is the songbird Area X striatal, pallidal, or both? an anatomical study , 2004, The Journal of comparative neurology.

[46]  Y. Smith,et al.  The output neurones and the dopaminergic neurones of the substantia nigra receive a GABA‐Containing input from the globus pallidus in the rat , 1990, The Journal of comparative neurology.

[47]  Sandra A. Brown,et al.  Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches , 1989, The Journal of comparative neurology.

[48]  Minmin Luo,et al.  A GABAergic, Strongly Inhibitory Projection to a Thalamic Nucleus in the Zebra Finch Song System , 1999, The Journal of Neuroscience.

[49]  C. Kitt,et al.  Projections of the paleostriatum upon the midbrain tegmentum in the pigeon , 1981, Neuroscience.

[50]  M. Gahr,et al.  Identification, distribution, and developmental changes of a melatonin binding site in the song control system of the zebra finch , 1996, The Journal of comparative neurology.

[51]  Robert C. Malenka,et al.  Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models , 2007, Nature.

[52]  D. Joel,et al.  The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum , 2000, Neuroscience.

[53]  F. Johnson,et al.  CB1 cannabinoid receptor expression in brain regions associated with zebra finch song control , 2000, Brain Research.

[54]  Long Ding,et al.  Long-Term Potentiation in an Avian Basal Ganglia Nucleus Essential for Vocal Learning , 2004, The Journal of Neuroscience.

[55]  O. Hikosaka Basal Ganglia Mechanisms of Reward‐Oriented Eye Movement , 2007, Annals of the New York Academy of Sciences.

[56]  J. Bolam,et al.  GABAB receptors at glutamatergic synapses in the rat striatum , 2005, Neuroscience.

[57]  D. Surmeier,et al.  Dichotomous Anatomical Properties of Adult Striatal Medium Spiny Neurons , 2008, The Journal of Neuroscience.

[58]  M. E. Anderson,et al.  Pallidal discharge related to the kinematics of reaching movements in two dimensions. , 1997, Journal of neurophysiology.

[59]  JM Tepper,et al.  GABAA receptor-mediated inhibition of rat substantia nigra dopaminergic neurons by pars reticulata projection neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  A. Reiner Functional circuitry of the avian basal ganglia: implications for basal ganglia organization in stem amniotes , 2002, Brain Research Bulletin.

[61]  T. Sotnikova,et al.  Social Context-Dependent Singing-Regulated Dopamine , 2006, The Journal of Neuroscience.

[62]  P. Deviche,et al.  Autoradiographic localization of opioid receptors in vocal control regions of a male passerine bird (Junco hyemalis) , 1995, The Journal of comparative neurology.

[63]  Y. Smith,et al.  Microcircuitry of the direct and indirect pathways of the basal ganglia. , 1998, Neuroscience.

[64]  A. Reiner,et al.  Identification of the Anterior Nucleus of the Ansa Lenticularis in Birds as the Homolog of the Mammalian Subthalamic Nucleus , 2000, The Journal of Neuroscience.

[65]  Abigail L. Person,et al.  Pallidal Neuron Activity Increases during Sensory Relay through Thalamus in a Songbird Circuit Essential for Learning , 2007, The Journal of Neuroscience.

[66]  Localization of met-enkephalin and vasoactive intestinal polypeptide in the brains of male zebra finches. , 1995, Brain, behavior and evolution.

[67]  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.

[68]  J. Rubenstein,et al.  Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx‐2, Emx‐1, Nkx‐2.1, Pax‐6, and Tbr‐1 , 2000, The Journal of comparative neurology.

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

[70]  O. Marín,et al.  Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. , 1999, Development.

[71]  N. M. Brooke,et al.  A molecular timescale for vertebrate evolution , 1998, Nature.

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

[73]  L. Medina,et al.  Subdivisions and derivatives of the chicken subpallium based on expression of LIM and other regulatory genes and markers of neuron subpopulations during development , 2009, The Journal of comparative neurology.

[74]  A. Doupe,et al.  Social context modulates singing-related neural activity in the songbird forebrain , 1999, Nature Neuroscience.

[75]  S. Nicola,et al.  Contrasting effects of dopamine and glutamate receptor antagonist injection in the nucleus accumbens suggest a neural mechanism underlying cue‐evoked goal‐directed behavior , 2004, The European journal of neuroscience.

[76]  S. Bottjer,et al.  The distribution of tyrosine hydroxylase immunoreactivity in the brains of male and female zebra finches. , 1993, Journal of neurobiology.

[77]  Michael A Farries,et al.  Organization of the songbird basal ganglia, including area X , 2008, The Journal of comparative neurology.

[78]  M. Farries,et al.  Evidence for “direct” and “indirect” pathways through the song system basal ganglia , 2005, The Journal of comparative neurology.

[79]  R. Llinás,et al.  Electrophysiological properties of guinea‐pig thalamic neurones: an in vitro study. , 1984, The Journal of physiology.

[80]  Martin Lévesque,et al.  Organization of the basal ganglia: the importance of axonal collateralization , 2000, Trends in Neurosciences.

[81]  A. Graybiel The basal ganglia: learning new tricks and loving it , 2005, Current Opinion in Neurobiology.

[82]  Gregory F Ball,et al.  Noradrenergic projections to the song control nucleus area X of the medial striatum in male zebra finches (Taeniopygia guttata) , 2007, The Journal of comparative neurology.

[83]  A. Parent,et al.  Two types of projection neurons in the internal pallidum of primates: Single‐axon tracing and three‐dimensional reconstruction , 2001, The Journal of comparative neurology.

[84]  S. Bottjer,et al.  An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch , 2004, The Journal of comparative neurology.

[85]  T. Wichmann,et al.  Neuronal activity in the primate substantia nigra pars reticulata during the performance of simple and memory-guided elbow movements. , 2004, Journal of neurophysiology.

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

[87]  F. Johnson,et al.  Zebra finch CB1 cannabinoid receptor: pharmacology and in vivo and in vitro effects of activation. , 2001, The Journal of pharmacology and experimental therapeutics.

[88]  P. Deviche,et al.  Age‐ and sex‐related differences in opioid receptor densities in the songbird vocal control system , 1999, The Journal of comparative neurology.

[89]  Samuel D. Gale,et al.  A novel basal ganglia pathway forms a loop linking a vocal learning circuit with its dopaminergic input , 2008, The Journal of comparative neurology.

[90]  W. Schultz Activity of pars reticulata neurons of monkey substantia nigra in relation to motor, sensory, and complex events. , 1986, Journal of neurophysiology.

[91]  A. Doupe,et al.  Contributions of an avian basal ganglia–forebrain circuit to real-time modulation of song , 2005, Nature.