Striatal cholinergic interneurons drive GABA release from dopamine terminals

Neuron

Volumn 82, Issue 1, 2014, Pages 63-70

  Nelson, Alexandra B ^a,b   Hammack, Nora ^a   Yang, Cindy F ^b   Shah, Nirao M ^b   Seal, Rebecca P ^c   Kreitzer, Anatol C ^a,b,d  

^a GLADSTONE INSTITUTES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; DOPAMINE; NICOTINIC RECEPTOR;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CHOLINERGIC NERVE CELL; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; CORPUS STRIATUM; GABAERGIC SYSTEM; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MOUSE; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; CHOLINE O-ACETYLTRANSFERASE; CORPUS STRIATUM; DOPAMINE; GAMMA-AMINOBUTYRIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROTRANSMITTER AGENTS; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; RECEPTORS, DOPAMINE D1; RHODOPSIN; SODIUM CHANNEL BLOCKERS;

EID: 84897954206     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.01.023     Document Type: Article

References (33)

1. Brown M.T., Tan K.R., O'Connor E.C., Nikonenko I., Muller D., Lüscher C. Ventral tegmental area GABA projections pause accumbal cholinergic interneurons to enhance associative learning. Nature 2012, 492:452-456.
2. Cachope R., Mateo Y., Mathur B.N., Irving J., Wang H.L., Morales M., Lovinger D.M., Cheer J.F. Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing. Cell Rep. 2012, 2:33-41.
3. Campbell K.J., Takada M., Hattori T. Co-localization of tyrosine hydroxylase and glutamate decarboxylase in a subpopulation of single nigrotectal projection neurons. Brain Res. 1991, 558:239-244.
4. Descarries L., Watkins K.C., Garcia S., Bosler O., Doucet G. Dual character, asynaptic and synaptic, of the dopamine innervation in adult rat neostriatum: a quantitative autoradiographic and immunocytochemical analysis. J. Comp. Neurol. 1996, 375:167-186.
5. English D.F., Ibanez-Sandoval O., Stark E., Tecuapetla F., Buzsáki G., Deisseroth K., Tepper J.M., Koos T. GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons. Nat. Neurosci. 2012, 15:123-130.
6. Exley R., Cragg S.J. Presynaptic nicotinic receptors: a dynamic and diverse cholinergic filter of striatal dopamine neurotransmission. Br. J. Pharmacol. 2008, 153(Suppl 1):S283-S297.
7. Gittis A.H., Nelson A.B., Thwin M.T., Palop J.J., Kreitzer A.C. Distinct roles of GABAergic interneurons in the regulation of striatal output pathways. J. Neurosci. 2010, 30:2223-2234.
8. González-Hernández T., Barroso-Chinea P., Acevedo A., Salido E., Rodríguez M. Colocalization of tyrosine hydroxylase and GAD65 mRNA in mesostriatal neurons. Eur. J. Neurosci. 2001, 13:57-67.
9. Hanley J.J., Bolam J.P. Synaptology of the nigrostriatal projection in relation to the compartmental organization of the neostriatum in the rat. Neuroscience 1997, 81:353-370.
10. Jones I.W., Bolam J.P., Wonnacott S. Presynaptic localisation of the nicotinic acetylcholine receptor beta2 subunit immunoreactivity in rat nigrostriatal dopaminergic neurones. J. Comp. Neurol. 2001, 439:235-247.
11. Karadsheh M.S., Shah M.S., Tang X., Macdonald R.L., Stitzel J.A. Functional characterization of mouse alpha4beta2 nicotinic acetylcholine receptors stably expressed in HEK293T cells. J. Neurochem. 2004, 91:1138-1150.
12. Kawaguchi Y. Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J. Neurosci. 1993, 13:4908-4923.
13. Kolisnyk B., Guzman M.S., Raulic S., Fan J., Magalhães A.C., Feng G., Gros R., Prado V.F., Prado M.A. ChAT-ChR2-EYFP mice have enhanced motor endurance but show deficits in attention and several additional cognitive domains. J. Neurosci. 2013, 33:10427-10438.
14. Koós T., Tepper J.M. Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat. Neurosci. 1999, 2:467-472.
15. Koós T., Tepper J.M. Dual cholinergic control of fast-spiking interneurons in the neostriatum. J. Neurosci. 2002, 22:529-535.
16. Lee S., Kim K., Zhou Z.J. Role of ACh-GABA cotransmission in detecting image motion and motion direction. Neuron 2010, 68:1159-1172.
17. Petreanu L., Gutnisky D.A., Huber D., Xu N.L., O'Connor D.H., Tian L., Looger L., Svoboda K. Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 2012, 489:299-303.
18. Rice M.E., Cragg S.J. Nicotine amplifies reward-related dopamine signals in striatum. Nat. Neurosci. 2004, 7:583-584.
19. Rice M.E., Cragg S.J. Dopamine spillover after quantal release: rethinking dopamine transmission in the nigrostriatal pathway. Brain Res. Brain Res. Rev. 2008, 58:303-313.
20. Shen W., Hamilton S.E., Nathanson N.M., Surmeier D.J. Cholinergic suppression of KCNQ channel currents enhances excitability of striatal medium spiny neurons. J. Neurosci. 2005, 25:7449-7458.
21. Shuen J.A., Chen M., Gloss B., Calakos N. Drd1a-tdTomato BAC transgenic mice for simultaneous visualization of medium spiny neurons in the direct and indirect pathways of the basal ganglia. J. Neurosci. 2008, 28:2681-2685.
22. Stuber G.D., Hnasko T.S., Britt J.P., Edwards R.H., Bonci A. Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J. Neurosci. 2010, 30:8229-8233.
23. Sullivan M.A., Chen H., Morikawa H. Recurrent inhibitory network among striatal cholinergic interneurons. J. Neurosci. 2008, 28:8682-8690.
24. 2+ release from stores. J. Neurosci. 2011, 31:13546-13561.
25. Threlfell S., Clements M.A., Khodai T., Pienaar I.S., Exley R., Wess J., Cragg S.J. Striatal muscarinic receptors promote activity dependence of dopamine transmission via distinct receptor subtypes on cholinergic interneurons in ventral versus dorsal striatum. J. Neurosci. 2010, 30:3398-3408.
26. Threlfell S., Lalic T., Platt N.J., Jennings K.A., Deisseroth K., Cragg S.J. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 2012, 75:58-64.
27. Tritsch N.X., Ding J.B., Sabatini B.L. Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 2012, 490:262-266.
28. Wilson C.J., Chang H.T., Kitai S.T. Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum. J. Neurosci. 1990, 10:508-519.
29. Witten I.B., Lin S.C., Brodsky M., Prakash R., Diester I., Anikeeva P., Gradinaru V., Ramakrishnan C., Deisseroth K. Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 2010, 330:1677-1681.
30. Yang C.F., Chiang M.C., Gray D.C., Prabhakaran M., Alvarado M., Juntti S.A., Unger E.K., Wells J.A., Shah N.M. Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell 2013, 153:896-909.
31. Zhang H., Sulzer D. Frequency-dependent modulation of dopamine release by nicotine. Nat. Neurosci. 2004, 7:581-582.
32. Zhao S., Ting J.T., Atallah H.E., Qiu L., Tan J., Gloss B., Augustine G.J., Deisseroth K., Luo M., Graybiel A.M., Feng G. Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nat. Methods 2011, 8:745-752.
33. Zhou F.M., Liang Y., Dani J.A. Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat. Neurosci. 2001, 4:1224-1229.