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

Journal of Chemical Neuroanatomy

Volumn 39, Issue 2, 2010, Pages 124-131

  Gale, Samuel D ^a   Perkel, David J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Anterior forebrain pathway; Area X; Dopamine; Pallidum; Striatum; Thalamus

Indexed keywords

4 AMINOBUTYRIC ACID; DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; ENKEPHALIN; SUBSTANCE P;

ANIMAL ANATOMY; BASAL GANGLION; BRAIN CORTEX; CELL TYPE; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; FOREBRAIN; FOWL; GLOBUS PALLIDUS; LEARNING; MAMMAL; NERVE CELL PLASTICITY; NEUROANATOMY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENSORIMOTOR FUNCTION; SONGBIRD; SPECIES DIFFERENCE; THALAMOCORTICAL TRACT; VOCALIZATION;

ANIMALS; BASAL GANGLIA; BIRDS; BRAIN; CATECHOLAMINES; GLOBUS PALLIDUS; LEARNING; NEURAL PATHWAYS; NEURONAL PLASTICITY; NEURONS; THALAMUS; VOCALIZATION, ANIMAL;

EID: 75349104436     PISSN: 08910618     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2009.07.003     Document Type: Review

References (91)

1. Abellán A., and Medina L. Subdivisions and derivatives of the chicken subpallium based on expression of LIM and other regulatory genes and markers of neuron subpopulations during development. J. Comp. Neurol. 515 (2009) 465-501
2. Anderson M.E., and Horak F.B. Influence of the globus pallidus on arm movements in monkeys. III. Timing of movement-related information. J. Neurophysiol. 54 (1985) 433-448
3. Bentley G.E. Melatonin receptor density in Area X of European starlings is correlated with reproductive state and is unaffected by plasma melatonin concentration. Gen. Comp. Endocrinol. 134 (2003) 187-192
4. Bentley G.E., and Ball G.F. Photoperiod-dependent and -independent regulation of melatonin receptors in the forebrain of songbirds. J. Neuroendocrinol. 12 (2000) 745-752
5. Bodor A.L., Giber K., Rovó Z., Ulbert I., and Acsády L. Structural correlates of efficient GABAergic transmission in the basal ganglia-thalamus pathway. J. Neurosci. 28 (2008) 3090-3102
6. Bottjer S.W., Halsema K.A., Brown S.A., and Miesner E.A. Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches. J. Comp. Neurol. 279 (1989) 312-326
7. Bottjer S.W. The distribution of tyrosine hydroxylase immunoreactivity in the brains of male and female zebra finches. J. Neurobiol. 24 (1993) 51-69
8. Bottjer S.W., and Alexander G. Localization of met-enkephalin and vasoactive intestinal polypeptide in the brains of male zebra finches. Brain Behav. Evol. 45 (1995) 153-177
9. Bottjer S.W., Roselinsky H., and Tran N.B. Sex differences in neuropeptide staining of song-control nuclei in zebra finch brains. Brain Behav. Evol. 50 (1997) 284-303
10. Brainard M.S., and Doupe A.J. Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404 (2000) 762-766
11. Carrillo G.D., and Doupe A.J. Is the songbird Area X striatal, pallidal, or both? An anatomical study. J. Comp. Neurol. 473 (2004) 415-437
12. Casto J.M., and Ball G.F. Characterization and localization of D1 dopamine receptors in the sexually dimorphic vocal control nucleus, area X, and the basal ganglia of European starlings. J. Neurobiol. 25 (1994) 767-780
13. Castelino C.B., and Ball G.F. A role for norepinephrine in the regulation of context-dependent ZENK expression in male zebra finches (Taeniopygia guttata). Eur. J. Neurosci. 21 (2005) 1962-1972
14. Castelino C.B., Diekamp B., and Ball G.F. Noradrenergic projections to the song control nucleus area X of the medial striatum in male zebra finches (Taeniopygia guttata). J. Comp. Neurol. 502 (2007) 544-562
15. Cepeda C., André V.M., Yamazaki I., Wu N., Kleiman-Weiner M., and Levine M.S. Differential electrophysiological properties of dopamine D1 and D2 receptor-containing striatal medium-sized spiny neurons. Eur. J. Neurosci. 27 (2008) 671-682
16. Chevalier G., and Deniau J.M. Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci. 13 (1990) 277-280
17. Ding L., and Perkel D.J. Dopamine modulates excitability of spiny neurons in the avian basal ganglia. J. Neurosci. 22 (2002) 5210-5218
18. Ding L., Perkel D.J., and Farries M.A. Presynaptic depression of glutamatergic synaptic transmission by D1-like dopamine receptor activation in the avian basal ganglia. J. Neurosci. 23 (2003) 6086-6095
19. Ding L., and Perkel D.J. Long-term potentiation in an avian basal ganglia nucleus essential for vocal learning. J. Neurosci. 24 (2004) 488-494
20. Doupe A.J. Song- and order-selective neurons in the songbird anterior forebrain and their emergence during vocal development. J. Neurosci. 17 (1997) 1147-1167
21. Doupe A.J., Perkel D.J., Reiner A., and Stern E.A. Birdbrains could teach basal ganglia research a new song. Trends Neurosci. 28 (2005) 353-363
22. Farries M.A., and Perkel D.J. A telencephalic nucleus essential for song learning contains neurons with physiological characteristics of both striatum and globus pallidus. J. Neurosci. 22 (2002) 3776-3787
23. Farries M.A., Ding L., and Perkel D.J. Evidence for "direct" and "indirect" pathways through the song system basal ganglia. J. Comp. Neurol. 484 (2005) 93-104
24. Fremeau Jr. R.T., Troyer M.D., Pahner I., Nygaard G.O., Tran C.H., Reimer R.J., Bellocchio E.E., Fortin D., Storm-Mathisen J., and Edwards R.H. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31 (2001) 247-260
25. Gahr M., and Kosar E. Identification, distribution, and developmental changes of a melatonin binding site in the control system of the zebra finch. J. Comp. Neurol. 367 (1996) 308-318
26. Gale S.D., Person A.L., and Perkel D.J. A novel basal ganglia pathway forms a loop linking a vocal learning circuit with its dopaminergic input. J. Comp. Neurol. 508 (2008) 824-839
27. Gertler T.S., Chan C.S., and Surmeier D.J. Dichotomous anatomical properties of adult striatal medium spiny neurons. J. Neurosci. 28 (2008) 10814-10824
28. Graybiel A.M. The basal ganglia: learning new tricks and loving it. Curr. Opin. Neurobiol. 15 (2005) 638-644
29. Graybiel A.M. Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 31 (2008) 359-381
30. Gulledge C.C., and DeViche P. Autoradiographic localization of opioid receptors in vocal control regions of a male passerine bird (Junco hyemalis). J. Comp. Neurol. 356 (1995) 408-417
31. Gulledge C.C., and DeViche P. Age-and sex-related differences in opioid receptor densities in the songbird vocal control system. J. Comp. Neurol. 404 (1999) 505-514
32. Hara E., Kubikova L., Hessler N.A., and Jarvis E.D. Role of the midbrain dopaminergic system in modulation of vocal brain activation by social context. Eur. J. Neurosci. 25 June (2007) 3406-3416
33. Hessler N.A., and Doupe A.J. Singing-related neural activity in a dorsal forebrain-basal ganglia circuit of adult zebra finches. J. Neurosci. 19 (1999) 10461-10481
34. Hessler N.A., and Doupe A.J. Social context modulates singing-related neural activity in the songbird forebrain. Nat. Neurosci. 2 (1999) 209-211
35. Hikosaka O., and Wurtz R.H. Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J. Neurophysiol. 49 (1983) 1285-1301
36. Hikosaka O., and Wurtz R.H. Modification of saccadic eye movements by GABA-related substances. II. Effects of muscimol in monkey substantia nigra pars reticulata. J. Neurophysiol. 53 (1985) 292-308
37. Hikosaka O. Basal ganglia mechanisms of reward-oriented eye movement. Ann. N. Y. Acad. Sci. 1104 (2007) 229-249
38. Jahnsen H., and Llinás R. Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J. Physiol. 349 (1984) 205-226
39. Jiao Y., Medina L., Veenman C.L., Toledo C., Puelles L., and Reiner A. Identification of the anterior nucleus of the ansa lenticularis in birds as the homolog of the mammalian subthalamic nucleus. J. Neurosci. 20 (2000) 6998-7010
40. Joel D., and Weiner I. 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. Neuroscience 96 (2000) 451-474
41. Kalivas P.W., Churchill L., and Klitenick M.L. GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area. Neuroscience 57 (1993) 1047-1060
42. Kao M.H., Doupe A.J., and Brainard M.S. Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 433 (2005) 638-643
43. Kao M.H., Wright B.D., and Doupe A.J. Neurons in a forebrain nucleus required for vocal plasticity rapidly switch between precise firing and variable bursting depending on social context. J. Neurosci. 28 (2008) 13232-13247
44. Kreitzer A.C., and Malenka R.C. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445 (2007) 643-647
45. Kreitzer A.C., and Malenka R.C. Striatal plasticity and basal ganglia circuit function. Neuron 60 (2008) 543-554
46. Kitt C.A., and Brauth S.E. Projections of the paleostriatum upon the midbrain tegmentum in the pigeon. Neuroscience 8 (1981) 1551-1566
47. Kojima S., and Doupe A.J. Activity propagation in an avian basal ganglia-thalamocortical circuit essential for vocal learning. J. Neurosci. 29 (2009) 4782-4793
48. Kumar S., and Hedges S.B. A molecular timescale for vertebrate evolution. Nature 392 (1998) 917-920
49. Lacey C.J., Boyes J., Gerlach O., Chen L., Magill P.J., and Bolam J.P. GABA(B) receptors at glutamatergic synapses in the rat striatum. Neuroscience 136 (2005) 1083-1095
50. Lewis J.W., Ryan S.M., Arnold A.P., and Butcher L.L. Evidence for a catecholaminergic projection to Area X in the zebra finch. J. Comp. Neurol. 196 (1981) 347-354
51. Llinás R.R., and Steriade M. Bursting of thalamic neurons and states of vigilance. J. Neurophysiol. 95 (2006) 3297-3308
52. Luo M., and Perkel D.J. Long-range GABAergic projection in a circuit essential for vocal learning. J. Comp. Neurol. 403 (1999) 68-84
53. Luo M., and Perkel D.J. A GABAergic, strongly inhibitory projection to a thalamic nucleus in the zebra finch song system. J. Neurosci. 19 (1999) 6700-6711
54. Medina L., and Reiner A. The efferent projections of the dorsal and ventral pallidal parts of the pigeon basal ganglia, studied with biotynylated dextran amine. Neuroscience 81 (1997) 773-802
55. Moss J., and Bolam J.P. A dopaminergic axon lattice in the striatum and its relationship with cortical and thalamic terminals. J. Neurosci. 28 (2008) 11221-11230
56. Nambu A., Tokuno H., Hamada I., Kita H., Imanishi M., Akazawa T., Ikeuchi Y., and Hasegawa N. Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J. Neurophysiol. 84 (2000) 289-300
57. Nevet A., Morris G., Saban G., Arkadir D., and Bergman H. Lack of spike-count and spike-time correlations in the substantia nigra reticulata despite overlap of neural responses. J. Neurophysiol. 98 (2007) 2232-2243
58. Nicola S.M., Surmeier J., and Malenka R.C. Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu. Rev. Neurosci. 23 (2000) 185-215
59. Ölveczky B.P., Andalman A.S., and Fee M.S. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol. 3 (2005) e153
60. Parent A., Sato F., Wu Y., Gauthier J., Levesque M., and Parent M. Organization of the basal ganglia: the importance of axonal collateralization. Trends Neurosci. 23 (2000) S20-27
61. Parent M., Lévesque M., and Parent A. Two types of projection neurons in the internal pallidum of primates: single-axon tracing and three-dimensional reconstruction. J. Comp. Neurol. 439 (2001) 162-175
62. Person A.L., and Perkel D.J. Unitary IPSPs drive precise thalamic spiking in a circuit required for learning. Neuron 46 (2005) 129-140
63. Person A.L., and Perkel D.J. Pallidal neuron activity increases during sensory relay through thalamus in a songbird circuit essential for learning. J. Neurosci. 27 (2007) 8686-8698
64. Person A.L., Gale S.D., Farries M.A., and Perkel D.J. Organization of the songbird basal ganglia, including Area X. J. Comp. Neurol. 508 (2008) 840-866
65. Puelles L., Kuwana E., Puelles E., Bulfone A., Shimamura K., Keleher J., Smiga S., and Rubenstein J.R. Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J. Comp. Neurol. 424 (2000) 409-438
66. Reiner A., Medina L., and Veenman C.L. Structural and functional evolution of the basal ganglia in vertebrates. Brain Res. Rev. 28 (1998) 235-285
67. Reiner A. Functional circuitry of the avian basal ganglia: implications for basal ganglia organization in stem amniotes. Brain Res. Bull. 57 (2002) 513-528
68. Reiner A., Perkel D.J., Bruce L.L., Butler A.B., Csillag A., Kuenzel W., Medina L., Paxinos G., Shimizu T., Striedter G., Wild M., Ball G.F., Durand S., Güntürkün O., Lee D.W., Mello C.V., Powers A., White S.A., Hough G., Kubikova L., Smulders T.V., Wada K., Dugas-Ford J., Husband S., Yamamoto K., Yu J., Siang C., Jarvis E.D., and Avian Brain Nomenclature Forum. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473 (2004) 377-414
69. Reiner A., Laverghetta A.V., Meade C.A., Cuthbertson S.L., and Bottjer S.W. An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch. J. Comp. Neurol. 469 (2004) 239-261
70. Ryan S.M., Arnold A.P., and Elde R.P. Enkephalin-like immunoreactivity in vocal control regions of the zebra finch brain. Brain Res. 229 (1981) 236-240
71. Sasaki A., Sotnikova T.D., Gainetdinov R.R., and Jarvis E.D. Social context-dependent singing-regulated dopamine. J. Neurosci. 26 (2006) 9010-9014
72. Scharff C., and Nottebohm F. A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning. J. Neurosci. 11 (1991) 2896-2913
73. Schultz W. Activity of pars reticulata neurons of monkey substantia nigra in relation to motor, sensory, and complex events. J. Neurophysiol. 55 (1986) 660-677
74. Schultz W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30 (2007) 259-280
75. Smith Y., and Bolam J.P. The output neurones and the dopaminergic neurones of the substantia nigra receive a GABA-containing input from the globus pallidus in the rat. J. Comp. Neurol. 296 (1990) 47-64
76. Smith Y., Bevan M.D., Shink E., and Bolam J.P. Microcircuitry of direct and indirect pathways of the basal ganglia. Neuroscience 86 (1998) 353-387
77. Smith Y., Raju D.V., Pare J.F., and Sidibé M. The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci. 27 (2004) 520-527
78. Soderstrom K., and Johnson F. CB1 cannabinoid receptor expression in brain regions associated with zebra finch song control. Brain Res. 857 (2000) 151-157
79. Soderstrom K., and Johnson F. Zebra finch CB1 cannabinoid receptor: pharmacology and in vivo and in vitro effects of activation. J. Pharmacol. Exp. Ther. 297 (2001) 189-197
80. Soderstrom K., and Johnson F. Cannabinoid exposure alters learning of zebra finch vocal patterns. Brain Res. 142 (2003) 215-217
81. Soha J.A., Shimizu T., and Doupe A.J. Development of the catecholaminergic innervation of the song system of the male zebra finch. J. Neurobiol. 29 (1996) 473-489
82. Sussel L., Marin O., Kimura S., and Rubenstein J.L. 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. Development 126 (1999) 3359-3370
83. Székely A.D., Boxer M.I., Stewart M.G., and Csillag A. Connectivity of the lobus parolfactorius of the domestic chicken (Gallus domesticus): an anterograde and retrograde pathway tracing study. J. Comp. Neurol. 348 (1994) 374-393
84. A receptor-mediated inhibition of rat substantia nigra dopaminergic neurons by pars reticulata projection neurons. J. Neurosci. 15 (1995) 3092-3103
85. Tepper J.M., and Lee C.R. GABAergic control of substantia nigra dopaminergic neurons. Prog. Brain Res. 160 (2007) 189-208
86. Turner R.S., and Anderson M.E. Pallidal discharge related to the kinematics of reaching movement in two dimensions. J. Neurophysiol. 77 (1997) 1051-1074
87. Vates G.E., Vicario D.S., and Nottebohm F. Reafferent thalamo-"cortical" loops in the song system of oscine songbirds. J. Comp. Neurol. 380 (1997) 275-290
88. Whitfield-Rucker M.G., and Cassone V.M. Melatonin binding in the house sparrow song control system: sexual dimorphism and the effect of photoperiod. Horm. Behav. 30 (1996) 528-537
89. Wichmann T., and Kliem M.A. Neuronal activity in the primate substantia nigra pars reticulata during the performance of simple and memory-guided elbow movements. J. Neurophysiol. 91 (2004) 815-827
90. Williams H., and Mehta N. Changes in adult zebra finch song require a forebrain nucleus that is not necessary for song production. J. Neurobiol. 39 (1990) 14-28
91. Yun I.A., Nicola S.M., and Fields H.L. Contrasting effects of dopamine and glutamate receptor antagonist injection in the nucleus accumbens suggest a neural mechanism underlying cue-evoked goal-directed behavior. Eur. J. Neurosci. 20 (2004) 249-263