Distinct roles of GABAergic interneurons in the regulation of striatal output pathways

Journal of Neuroscience

Volumn 30, Issue 6, 2010, Pages 2223-2234

  Gittis, Aryn H ^a   Nelson, Alexandra B ^a   Thwin, Myo T ^a   Palop, Jorge J ^a   Kreitzer, Anatol C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; LIM HOMEOBOX PROTEIN 6; N METHYL DEXTRO ASPARTIC ACID; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL POPULATION; CELL STRUCTURE; ELECTROPHYSIOLOGY; EXCITATORY JUNCTION POTENTIAL; INTERNEURON; MEDIUM SPINY NEURON; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; STRIATE CORTEX; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

ACTION POTENTIALS; ANIMALS; CORPUS STRIATUM; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; MICE; MICE, TRANSGENIC; NEURAL INHIBITION; NEURAL PATHWAYS; PATCH-CLAMP TECHNIQUES; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 76649130165     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4870-09.2010     Document Type: Article

References (57)

1. Abbott LF, Varela JA, Sen K, Nelson SB (1997) Synaptic depression and cortical gain control. Science 275:220 -224.
2. Aoki C, Pickel VM (1989) Neuropeptide Y in the cerebral cortex and the caudate-putamen nuclei: ultrastructural basis for interactions with GABAergic and non-GABAergic neurons. J Neurosci 9:4333- 4354.
3. Aoki C, Pickel VM (1990) Neuropeptide Y in cortex and striatum. Ultrastructural distribution and coexistence with classical neurotransmitters and neuropeptides. Ann N Y Acad Sci 611:186 -205.
4. Arenz A, Silver RA, Schaefer AT, Margrie TW (2008) The contribution of single synapses to sensory representation in vivo. Science 321:977-980.
5. Bagnall MW, McElvain LE, Faulstich M, du Lac S (2008) Frequencyindependent synaptic transmission supports a linear vestibular behavior. Neuron 60:343-352.
6. Berke JD (2008) Uncoordinated firing rate changes of striatal fast-spiking interneurons during behavioral task performance. J Neurosci 28:10075-10080.
7. Berke JD, Okatan M, Skurski J, Eichenbaum HB (2004) Oscillatory entrainment of striatal neurons in freely moving rats. Neuron 43:883- 896.
8. Blackwell KT, Czubayko U, Plenz D (2003) Quantitative estimate of synaptic inputs to striatal neurons during up and down states in vitro. J Neurosci 23:9123-9132.
9. Cobos I, Long JE, Thwin MT, Rubenstein JL (2006) Cellular patterns of transcription factor expression in developing cortical interneurons. Cereb Cortex 16 (Suppl 1):i82-i88.
10. Dehorter N, Guigoni C, Lopez C, Hirsch J, Eusebio A, Ben-Ari Y, Hammond C (2009) Dopamine-deprived striatal GABAergic interneurons burst and generate repetitive gigantic IPSCs in medium spiny neurons. J Neurosci 29:7776 -7787.
11. de Kock CP, Bruno RM, Spors H, Sakmann B (2007) Layer- and cell-typespecific suprathreshold stimulus representation in rat primary somatosensory cortex. J Physiol 581:139 -154.
12. Dittman JS, Regehr WG (1998) Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18:6147- 6162.
13. Figueredo-Cardenas G, Medina L, Reiner A (1996) Calretinin is largely localized to a unique population of striatal interneurons in rats. Brain Res 709:145-150.
14. Földy C, Lee SY, Szabadics J, Neu A, Soltesz I (2007) Cell type-specific gating of perisomatic inhibition by cholecystokinin. Nat Neurosci 10:1128-1130.
15. Gabernet L, Jadhav SP, Feldman DE, Carandini M, ScanzianiM (2005) Somatosensory integration controlled by dynamic thalamocortical feedforward inhibition. Neuron 48:315-327.
16. Galarraga E, Vilchis C, Tkatch T, Salgado H, Tecuapetla F, Perez-Rosello T, Perez-Garci E, Hernandez-Echeagaray E, Surmeier DJ, Bargas J (2007) Somatostatinergic modulation of firing pattern and calcium-activated potassium currents in medium spiny neostriatal neurons. Neuroscience 146:537-554.
17. Galarreta M, Hestrin S (1998) Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat Neurosci 1:587-594.
18. Galvan A, Wichmann T (2007) GABAergic circuits in the basal ganglia and movement disorders. Prog Brain Res 160:287-312.
19. Gernert M, Hamann M, Bennay M, Löscher W, Richter A (2000) Deficit of striatal parvalbumin-reactive GABAergic interneurons and decreased basal ganglia output in a genetic rodent model of idiopathic paroxysmal dystonia. J Neurosci 20:7052-7058.
20. Gertler TS, Chan CS, Surmeier DJ (2008) Dichotomous anatomical properties of adult striatal medium spiny neurons. J Neurosci 28:10814-10824.
21. Graybiel AM, Canales JJ, Capper-Loup C (2000) Levodopa-induced dyskinesias and dopamine-dependent stereotypies: a new hypothesis. Trends Neurosci 23:S71-77.
22. Isaac JT, Ashby M, McBain CJ (2007) The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54:859-871.
23. Kalanithi PS, Zheng W, Kataoka Y, DiFiglia M, Grantz H, Saper CB, Schwartz ML, Leckman JF, Vaccarino FM (2005) Altered parvalbumin-positive neuron distribution in basal ganglia of individuals with Tourette syndrome. Proc Natl Acad Sci U S A 102:13307-13312.
24. Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908-4923.
25. Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC (1995) Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18:527-535.
26. Koós T, Tepper JM (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2:467- 472.
27. Koos T, Tepper JM, Wilson CJ (2004) Comparison of IPSCs evoked by spiny and fast-spiking neurons in the neostriatum. J Neurosci 24:7916-7922.
28. Kreitzer AC (2009) Physiology and pharmacology of striatal neurons. Annu Rev Neurosci 32:127-147.
29. Kreitzer AC, MalenkaRC (2007) Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445:643- 647.
30. Kreitzer AC, Malenka RC (2008) Striatal plasticity and basal ganglia circuit function. Neuron 60:543-554.
31. Kubota Y, Kawaguchi Y (2000) Dependence of GABAergic synaptic areas on the interneuron type and target size. J Neurosci 20:375-386.
32. Lopez-Huerta VG, Tecuapetla F, Guzman JN, Bargas J, Galarraga E (2008) Presynaptic modulation by somatostatin in the neostriatum. Neurochem Res 33:1452-1458.
33. Mallet N, Le Moine C, Charpier S, Gonon F (2005) Feedforward inhibition of projection neurons by fast-spiking GABA interneurons in the rat striatum in vivo. J Neurosci 25:3857-3869.
34. 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.
35. Marin O, Anderson SA, Rubenstein JL (2000) Origin and molecular specification of striatal interneurons. J Neurosci 20:6063- 6076.
36. Markram H, Gupta A, Uziel A, Wang Y, Tsodyks M (1998) Information processing with frequency-dependent synaptic connections. Neurobiol Learn Mem 70:101-112.
37. McBain CJ, Fisahn A (2001) Interneurons unbound. Nat Rev Neurosci 2:11-23.
38. Mura A, Linder JC, Young SJ, Groves PM (2000) Striatal cells containing aromatic L-amino acid decarboxylase: an immunohistochemical comparison with other classes of striatal neurons. Neuroscience 98:501-511.
39. Nisenbaum ES, Berger TW (1992) Functionally distinct subpopulations of striatal neurons are differentially regulated by GABAergic and dopaminergic inputs-I. In vivo analysis. Neuroscience 48:561-578.
40. O'Donnell P, GraceAA (1997) Cortical afferents modulate striatal gap junction permeability via nitric oxide. Neuroscience 76:1-5.
41. Palop JJ, Chin J, Bien-Ly N, Massaro C, Yeung BZ, Yu GQ, Mucke L (2005) Vulnerability of dentate granule cells to disruption of arc expression in human amyloid precursor protein transgenic mice. J Neurosci 25:9686-9693.
42. Parthasarathy HB, Graybiel AM (1997) Cortically driven immediate-early gene expression reflects modular influence of sensorimotor cortex on identified striatal neurons in the squirrel monkey. J Neurosci 17:2477-2491.
43. Ramanathan S, Hanley JJ, Deniau JM, Bolam JP (2002) Synaptic convergence of motor and somatosensory cortical afferents onto GABAergic interneurons in the rat striatum. J Neurosci 22:8158-8169.
44. Shuen JA, Chen M, Gloss B, CalakosN (2008) Drd1a-tdTomato BAC transgenic mice for simultaneous visualization of medium spiny neurons in the direct and indirect pathways of the basal ganglia. J Neurosci 28:2681-2685.
45. Smith Y, Bevan MD, Shink E, Bolam JP (1998) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86:353-387.
46. Steinert JR, Kopp-Scheinpflug C, Baker C, Challiss RA, Mistry R, Haustein MD, Griffin SJ, Tong H, Graham BP, Forsythe ID (2008) Nitric oxide is a volume transmitter regulating postsynaptic excitability at a glutamatergic synapse. Neuron 60:642- 656.
47. Taverna S, Canciani B, PennartzCM (2007) Membrane properties and synaptic connectivity of fast-spiking interneurons in rat ventral striatum. Brain Res 1152:49 -56.
48. Telgkamp P, Raman IM (2002) Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei. J Neurosci 22:8447- 8457.
49. Tepper JM, Bolam JP (2004) Functional diversity and specificity of neostriatal interneurons. Curr Opin Neurobiol 14:685- 692.
50. Tepper JM, Koós T, Wilson CJ (2004) GABAergic microcircuits in the neostriatum. Trends Neurosci 27:662- 669.
51. Theriault E, Landis DM (1987) Morphology of striatal neurons containing VIP-like immunoreactivity. J Comp Neurol 256:1-13.
52. Varela JA, Song S, Turrigiano GG, Nelson SB (1999) Differential depression at excitatory and inhibitory synapses in visual cortex. J Neurosci 19:4293- 4304.
53. West AR, Grace AA (2004) The nitric oxide-guanylyl cyclase signaling pathway modulates membrane activity States and electrophysiological properties of striatal medium spiny neurons recorded in vivo. J Neurosci 24:1924 -1935.
54. West AR, Galloway MP, Grace AA (2002) Regulation of striatal dopamine neurotransmission by nitric oxide: effector pathways and signaling mechanisms. Synapse 44:227-245.
55. Wilson CJ (1998) The synaptic organization of the brain, Ed 4. Oxford: Oxford Scholarship.
56. Wilson CJ (2007) GABAergic inhibition in the neostriatum. Prog Brain Res 160:91-110.
57. Wu Y, Parent A (2000) Striatal interneurons expressing calretinin, parvalbumin or NADPH-diaphorase: a comparative study in the rat, monkey and human. Brain Res 863:182-191.