Millisecond timescale disinhibition mediates fast information transmission through an avian basal ganglia loop

Journal of Neuroscience

Volumn 29, Issue 49, 2009, Pages 15420-15433

  Leblois, Arthur ^a   Bodor, Ágnes L ^a   Person, Abigail L ^a,b   Perkel, David J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMATE RECEPTOR;

ACCURACY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN CORTEX; BRAIN DEPTH STIMULATION; BRAIN NERVE CELL; BRAIN NUCLEUS; ELECTROSTIMULATION; EVOKED RESPONSE; FOWL; IN VIVO STUDY; LATENT PERIOD; LEARNING; MALE; MOTOR ACTIVITY; NEUROTRANSMISSION; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROBABILITY; SENSORY NERVE; SIGNAL TRANSDUCTION; SONGBIRD; STRIATE CORTEX; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; THALAMOCORTICAL TRACT; THALAMUS NUCLEUS; THEORETICAL MODEL; VERBAL COMMUNICATION; VOCALIZATION;

ACTION POTENTIALS; ANIMALS; BASAL GANGLIA; CEREBRAL CORTEX; ELECTRIC STIMULATION; FINCHES; MALE; MODELS, NEUROLOGICAL; NEURAL INHIBITION; NEURAL PATHWAYS; NEURONS; PROBABILITY; RECEPTORS, GLUTAMATE; SYNAPTIC TRANSMISSION; THALAMUS; TIME FACTORS;

EID: 71849106693     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3060-09.2009     Document Type: Article

References (64)

1. Aosaki T, Tsubokawa H, Ishida A, Watanabe K, Graybiel AM, Kimura M (1994) Responses of tonically active neurons in the primate's striatum undergo systematic changes during behavioral sensorimotor conditioning. J Neurosci 14:3969-3984. (Pubitemid 24174138)
2. Bagshaw EV, Evans MH (1976) Measurement of current spread from microelectrodes when stimulating within the nervous system. Exp Brain Res 25:391-400.
3. Baker SN, Gerstein GL (2001) Determination of response latency and its application to normalization of cross-correlation measures. Neurol Comput 13:1351-1377.
4. Bodor AL, Giber K, Rovó Z, Ulbert I, Acsády L (2008) Structural correlates of efficient GABAergic transmission in the basal ganglia-thalamus pathway. J Neurosci 28:3090-3102.
5. Bottjer SW, Miesner EA, Arnold AP (1984) Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224:901-903.
6. Bottjer SW, Halsema KA, Brown SA, Miesner EA (1989) Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches. J Comp Neurol 279:312-326.
7. Broussard DM, Brontë-Stewart HM, Lisberger SG (1992) Expression of motor learning in the response of the primate vestibuloocular reflex pathway to electrical stimulation. J Neurophysiol 67:1493-1508.
8. Carrillo GD, Doupe AJ (2004) Is the songbird Area X striatal, pallidal, or both? An anatomical study. J Comp Neurol 473:415-437.
9. Charpier S, Mahon S, Deniau JM (1999) In vivo induction of striatal long-term potentiation by low-frequency stimulation of the cerebral cortex. Neuroscience 91:1209-1222.
10. Deniau JM, Chevalier G (1985) Disinhibition as a basic process in the expression of striatal functions. II. The striato-nigral influence on thalamocortical cells of the ventromedial thalamic nucleus. Brain Res 334:227-233.
11. Destexhe A, Bal T, McCormick DA, Sejnowski TJ (1996) Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. J Neurophysiol 76:2049-2070. (Pubitemid 26322639)
12. Ding L, Perkel DJ (2004) Long-term potentiation in an avian basal ganglia nucleus essential for vocal learning. J Neurosci 24:488-494. (Pubitemid 38112380)
13. Farries MA, Perkel DJ (2002) A telencephalic nucleus essential for song learning contains neurons with physiological characteristics of both striatum and globus pallidus. J Neurosci 22:3776-3787.
14. Farries MA, Ding L, Perkel DJ (2005) Evidence for "direct" and "indirect" pathways through the song system basal ganglia. J Comp Neurol 484:93-104. (Pubitemid 40326233)
15. Follett KA, Mann MD (1986) Effective stimulation distance for current from macroelectrodes. Exp Neurol 92:75-91.
16. Foster EF, Mehta RP, Bottjer SW (1997) Axonal connections of the medial magnocellular nucleus of the anterior neostriatum in zebra finches. J Comp Neurol 382:364-381.
17. Gale SD, Person AL, Perkel DJ (2008) A novel basal ganglia pathway forms a loop linking a vocal learning circuit with its dopaminergic input. J Comp Neurol 508:824-839.
18. Glaze CM, Troyer TW (2007) Behavioral measurements of a temporally precise motor code for birdsong. J Neurosci 27:7631-7639.
19. Goller F, Cooper BG (2004) Peripheral motor dynamics of song production in the zebra finch. Ann NY Acad Sci 1016:130-152. (Pubitemid 38951464)
20. Graybiel AM (2005) The basal ganglia: learning new tricks and loving it. Curr Opin Neurobiol 15:638-644. (Pubitemid 41683155)
21. Hahnloser RH, Kozhevnikov AA, Fee MS (2002) An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419:65-70.
22. Hahnloser RH, Kozhevnikov AA, Fee MS (2006) Sleep-related neural activity in a premotor and a basal-ganglia pathway of the songbird. J Neurophysiol 96:794-812.
23. Heil P, Scheich H (1991) Functional organization of the avian auditory cortex analogue. II. Topographic distribution of latency. Brain Res 539: 121-125.
24. Hines ML (1998) The neurosimulator NEURON. In: Methods in neuronal modeling (Koch C, Segev I, eds), pp 129-136. Cambridge, MA: MIT.
25. Jarvis ED, Güntürkün O, Bruce L, Csillag A, Karten H, Kuenzel W, Medina L, Paxinos G, Perkel DJ, Shimizu T, Striedter G, Wild JM, Ball GF, Dugas-Ford J, Durand SE, Hough GE, Husband S, Kubikova L, Lee DW, Mello CV, Powers A, Siang C, Smulders TV, Wada K, White SA, Yamamoto K, Yu J, Reiner A, Butler AB (2005) Avian brain nomenclature consortium. Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6:151-159.
26. Kao MH, Doupe AJ, Brainard MS (2005) Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 433:638-643.
27. Kao MH, Wright BD, Doupe AJ (2008) Neurons in a forebrain nucleus required for vocal plasticity rapidly switch between precise firing and variable bursting depending on social context. J Neurosci 28:13232-13247.
28. Kimpo RR, Theunissen FE, Doupe AJ (2003) Propagation of correlated activity through multiple stages of a neural circuit. J Neurosci 23:5750-5761.
29. Kojima S, Doupe AJ (2009) Activity propagation in an avian basal ganglia-thalamocortical circuit essential for vocal learning. J Neurosci 29:4782-4793.
30. Kozhevnikov AA, Fee MS (2007) Singing-related activity of identified HVC neurons in the zebra finch. J Neurophysiol 97:4271-4283.
31. Kubota M, Saito N (1991) NMDA receptors participate differentially in two different synaptic inputs in neurons of the zebra finch robust nucleus of the archistriatum in vitro. Neurosci Lett 125:107-109.
32. Liberman AM, Harris KS, Kinney JA, Lane H (1961) The discrimination of relative onset-time of the components of certain speech and nonspeech patterns. J Exp Psychol 61:379-388.
33. Luo M, Perkel DJ (1999a) Long-range GABAergic projection in a circuit essential for vocal learning. J Comp Neurol 403:68-84. (Pubitemid 28553334)
34. Luo M, Perkel DJ (1999b) A GABAergic, strongly inhibitory projection to a thalamic nucleus in the zebra finch song system. J Neurosci 19:6700-6711. (Pubitemid 29347470)
35. Luo M, Perkel DJ (2002) Intrinsic and synaptic properties of neurons in an avian thalamic nucleus during song learning. J Neurophysiol 88:1903-1914. (Pubitemid 35191191)
36. MacDougall-Shackleton SA, Hulse SH, Ball GF (1998) Neural correlates of singing behavior in male zebra finches (Taeniopygia guttata). J Neurobiol 36:421-430. (Pubitemid 28397151)
37. Maggi CA, Meli A (1986) Suitability of urethane anesthesia for physiopharmacological investigations in various systems. I. General considerations. Experentia 42:109-114.
38. Mallet N, Ballion B, Le Moine C, Gonon F (2006) Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of Parkinsonian rats. J Neurosci 26:3875-3884.
39. McCormick DA, Huguenard JR (1992) A model of the electrophysiological properties of thalamocortical relay neurons. J Neurophysiol 68:1384-1400.
40. Mooney R (1992) Synaptic basis for developmental plasticity in a birdsong nucleus. J Neurosci 12:2464-2477.
41. Mooney R, Konishi M (1991) Two distinct inputs to an avian song nucleus activate different glutamate receptor subtypes on individual neurons. Proc Natl Acad Sci U S A 88:4075-4079. (Pubitemid 21914481)
42. Nambu A, Tokuno H, Hamada I, Kita H, Imanishi M, Akazawa T, Ikeuchi Y, HasegawaN (2000) Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J Neurophysiol 84:289-300.
43. Nottebohm F, Stokes TM, Leonard CM (1976) Central control of song in the canary, Serinus canarius. J Comp Neurol 165:457-486.
44. Okuhata S, Saito N (1987) Synaptic connections of thalamo-cerebral vocal nuclei of the canary. Brain Res Bull 18:35-44. (Pubitemid 17017495)
45. Olveczky BP, Andalman AS, Fee MS (2005) Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol 3:e153.
46. Person AL, Perkel DJ (2005) Unitary IPSPs drive precise thalamic spiking in a circuit required for learning. Neuron 46:129-140.
47. Person AL, Perkel DJ (2007) Pallidal neuron activity increases during sensory relay through thalamus in a songbird circuit essential for learning. J Neurosci 27:8687-8698.
48. Person AL, Gale SD, Farries MA, Perkel DJ (2008) Organization of the song-bird basal ganglia, including Area X. J Comp Neurol 508:840-866.
49. Pollak GD, Burger RM, Klug A (2003) Dissecting the circuitry of the auditory system. Trends Neurosci 26:33-39.
50. Ranck JB Jr (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98:417-440.
51. Reiner A, Laverghetta AV, Meade CA, Cuthbertson SL, Bottjer SW (2004a) An immunohistochemical and pathway tracing study of the striatopallidal organization of Area X in the male zebra finch. J Comp Neurol 469:239-261. (Pubitemid 38083873)
52. Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Güntürkün O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED, Gütürkün O (2004b) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377-414. (Pubitemid 38580457)
53. Sasaki A, Sotnikova TD, Gainetdinov RR, Jarvis ED (2006) Social context-dependent singing-regulated dopamine. J Neurosci 26:9010-9014.
54. Scharff C, Nottebohm F (1991) A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning. J Neurosci 11:2896-2913.
55. Sen K, Theunissen FE, Doupe AJ (2001) Feature analysis of natural sounds in the songbird auditory forebrain. J Neurophysiol 86:1445-1458. (Pubitemid 32847788)
56. Somogyi P, Hodgson AJ (1985) Antisera to gamma-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. J Histochem Cytochem 33:249-257. (Pubitemid 15130013)
57. Stark LL, Perkel DJ (1999) Two-stage, input-specific synaptic maturation in a nucleus essential for vocal production in the zebra finch. J Neurosci 19:9107-9116.
58. Tehovnik EJ, Tolias AS, Sultan F, SlocumWM,LogothetisNK (2006) Direct and indirect activation of cortical neurons by electrical microstimulation. J Neurophysiol 96:512-521. (Pubitemid 44155190)
59. Thomson AM (1988) Inhibitory postsynaptic potentials evoked in thalamic neurons by stimulation of the reticularis nucleus evoke slow spikes in isolated rat brain slices. I. Neuroscience 25:491-502.
60. Troyer TW, Doupe AJ (2000) An associational model of birdsong sensorimotor learning I. Efference copy and the learning of song syllables. J Neurophysiol 84:1204-1223. (Pubitemid 30688147)
61. Vates GE, Vicario DS, Nottebohm F (1997) Reafferent thalamo- "cortical" loops in the song system of oscine songbirds. J Comp Neurol 380: 275-290.
62. Wanaverbecq N, Bodor AL, Bokor H, Slézia A, Lüthi A, Acsády L (2008) Contrasting the functional properties of GABAergic axon terminals with single and multiple synapses in the thalamus. J Neurosci 28:11848-11861.
63. Wild JM (1993) Descending projections of the songbird nucleus robustus archistriatalis. J Comp Neurol 338:225-241.
64. Wild JM, Williams MN, Howie GJ, Mooney R (2005) Calcium-binding proteins define interneurons inHVCof the zebra finch (Taeniopygia guttata). J Comp Neurol 483:76-90.