Phasic dopaminergic activity exerts fast control of cholinergic interneuron firing via sequential NMDA, D2, and D1 receptor activation

Journal of Neuroscience

Volumn 34, Issue 35, 2014, Pages 11549-11559

  Wieland, Sebastian ^a   Du, Dan ^a   Oswald, Manfred J ^a   Parlato, Rosanna ^a,b   Köhr, Georg ^a   Kelsch, Wolfgang ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

Cholinergic interneurons; Glutamate corelease; Olfactory tubercle; Pause response; Phasic dopamine; Striatum

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL) PYRIDAZINIUM BROMIDE; 3 AMINOPROPYL (DIETHOXYMETHYL) PHOSPHINIC ACID; 6 CYANO 7 NITRO 2, 3 QUINOXALINEDIONE; 8 CHLORO 2, 3, 4, 5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; ATROPINE; DIHYDRO BETA ERYTHROIDINE; DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; SULPIRIDE; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CHOLINERGIC INTERNEURON FIRING; CONTROLLED STUDY; DOPAMINERGIC ACTIVITY; ELECTROPHYSIOLOGY; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE STEADY POTENTIAL; MOUSE; NEUROLOGICAL AND SENSORIAL PROCEDURES; NONHUMAN; POTENTIOMETRY; PRIORITY JOURNAL; SYNAPSE; WHOLE CELL PATCH CLAMP;

CHOLINERGIC INTERNEURONS; GLUTAMATE CORELEASE; OLFACTORY TUBERCLE; PAUSE RESPONSE; PHASIC DOPAMINE; STRIATUM;

ANIMALS; BASAL GANGLIA; CHOLINERGIC NEURONS; DOPAMINERGIC NEURONS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84906535672     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1175-14.2014     Document Type: Article

References (61)

1. Aosaki T., Graybiel AM, KimuraM (1994a) Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys. Science 265:412-415. CrossRef Medline
2. Aosaki T., Tsubokawa H, Ishida A, Watanabe K, Graybiel AM, Kimura M (1994b) Responses of tonically active neurons in the primate's striatum undergo systematic changes during behavioral sensorimotor conditioning. J Neurosci 14:3969-3984. Medline
3. Aosaki T., Kiuchi K, Kawaguchi Y (1998) Dopamine D1-like receptor activation excites rat striatal large aspiny neurons in vitro. J Neurosci 18: 5180-5190. Medline
4. Apicella P., Ravel S, Deffains M, Legallet E (2011) The role of striatal tonically active neurons in reward prediction error signaling during instrumental task performance. J Neurosci 31:1507-1515. CrossRef Medline
5. Atallah H. E, McCool AD, Howe MW, Graybiel AM (2014) Neurons in the ventral striatum exhibit cell-type-specific representations of outcome during learning. Neuron 82:1145-1156. CrossRef Medline
6. Beatty J. A, Sullivan MA, Morikawa H, Wilson CJ (2012) Complex autonomous firing patterns of striatal low-threshold spike interneurons. J Neurophysiol 108:771-781. CrossRef Medline
7. Been L. E, Staffend NA, Tucker A, Meisel RL (2013) Vesicular glutamate transporter 2 and tyrosine hydroxylase are not co-localized in Syrian hamster nucleus accumbens afferents. Neurosci Lett 550:41-45. CrossRef Medline
8. Benhamou L., Kehat O, Cohen D (2014) Firing pattern characteristics of tonically active neurons in rat striatum: context dependent or species divergent? J Neurosci 34:2299-2304. CrossRef Medline
9. Berridge K. C, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28:309-369. CrossRef Medline
10. Bromberg-Martin E. S, Matsumoto M, HikosakaO (2010) Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68:815-834. CrossRef Medline
11. Cardin J. A, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore C. I (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459:663-667. CrossRef Medline
12. Centonze D., Grande C, Usiello A, Gubellini P, Erbs E, Martin AB, Pisani A, Tognazzi N., Bernardi G, Moratalla R, Borrelli E, Calabresi P (2003) Receptor subtypes involved in the presynaptic and postsynaptic actions of dopamine on striatal interneurons. J Neurosci 23:6245-6254. Medline
13. Chuhma N., Zhang H, Masson J, Zhuang X, Sulzer D, Hen R, Rayport S (2004) Dopamine neurons mediate a fast excitatory signal via their glutamatergic synapses. J Neurosci 24:972-981. CrossRef Medline
14. Chuhma N., Mingote S, Moore H, Rayport S (2014) Dopamine neurons control striatal cholinergic neurons via regionally heterogeneous dopamine and glutamate signaling. Neuron 81:901-912. CrossRef Medline
15. Cohen J. Y, Haesler S, Vong L, Lowell BB, Uchida N (2012) Neuron-typespecific signals for reward and punishment in the ventral tegmental area. Nature 482:85-88. CrossRef Medline
16. Deng P., Zhang Y, Xu ZC (2007) Involvement of I(h) in dopamine modulation of tonic firing in striatal cholinergic interneurons. J Neurosci 27: 3148-3156. CrossRef Medline
17. Descarries L., Bérubé-Carrière N, Riad M, Bo GD, Mendez JA, Trudeau LE (2008) Glutamate in dopamine neurons: synaptic versus diffuse transmission. Brain Res Rev 58:290-302. CrossRef Medline
18. Dimova R., Vuillet J, Nieoullon A, Kerkerian-Le Goff L (1993) Ultrastructural features of the choline acetyltransferase-containing neurons and relationships with nigral dopaminergic and cortical afferent pathways in the rat striatum. Neuroscience 53:1059-1071. CrossRef Medline
19. Ding J. B, Guzman JN, Peterson JD, Goldberg JA, Surmeier DJ (2010) Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron 67:294-307. CrossRef Medline
20. Doig N.M, Magill PJ, Apicella P, Bolam JP, Sharott A (2014) Cortical and thalamic excitation mediate the multiphasic responses of striatal cholinergic interneurons to motivationally salient stimuli. J Neurosci 34:3101-3117. CrossRef Medline
21. English D. F, Ibanez-Sandoval O, Stark E, Tecuapetla F, Buzsáki G, Deisseroth K, Tepper JM, Koos T (2012) GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons. Nat Neurosci 15:123-130. CrossRef
22. Grace A. A (1991) Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 41:1-24. CrossRef Medline
23. Haberly L. B, Price JL (1978) Association and commissural fiber systems of the olfactory cortex of the rat. J Comp Neurol 178:711-740. CrossRef Medline
24. Hnasko T. S, Chuhma N, Zhang H, Goh GY, Sulzer D, Palmiter RD, Rayport S, Edwards R. H (2010) Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo. Neuron 65:643-656. CrossRef Medline
25. Hnasko T. S, Hjelmstad GO, Fields HL, Edwards RH (2012) Ventral tegmental area glutamate neurons: electrophysiological properties and projections. J Neurosci 32:15076-15085. CrossRef Medline
26. Ikemoto S. (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56:27-78. CrossRef Medline
27. Kapur S. (2003) Psychosis as a state of aberrant salience: A framework linking biology, phenomenology, and pharmacology in schizophrenia. Am J Psychiatry 160:13-23. CrossRef Medline
28. Kawaguchi Y. (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908-4923. Medline
29. Kimura M., Rajkowski J, Evarts E (1984) Tonically discharging putamen neurons exhibit set-dependent responses. Proc Natl Acad Sci U S A 81: 4998-5001. CrossRef Medline
30. Kreitzer A. C (2009) Physiology and pharmacology of striatal neurons. Annu Rev Neurosci 32:127-147. CrossRef Medline
31. Lapper S. R, Bolam JP (1992) Input from the frontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat. Neuroscience 51:533-545. CrossRef Medline
32. Ljungberg T., Apicella P, SchultzW (1992) Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 67:145-163. Medline
33. Matsuda W., Furuta T, Nakamura KC, Hioki H, Fujiyama F, Arai R, Kaneko T (2009) Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J Neurosci 29:444-453. CrossRef Medline
34. Maurice N., Mercer J, Chan CS, Hernandez-Lopez S, Held J, Tkatch T, Surmeier DJ (2004) D2 dopamine receptor-mediated modulation of voltage-dependent Na+ channels reduces autonomous activity in striatal cholinergic interneurons. J Neurosci 24:10289-10301. CrossRef Medline
35. McNamara A. M, Cleland TA, Linster C (2004) Characterization of the synaptic properties of olfactory bulb projections. Chem Senses 29:225-233. CrossRef Medline
36. Millhouse O. E, Heimer L (1984) Cell configurations in the olfactory tubercle of the rat. J Comp Neurol 228:571-597. CrossRef Medline
37. Monory K., Massa F, Egertová M, Eder M, Blaudzun H, Westenbroek R, Kelsch W., Jacob W, Marsch R, Ekker M, Long J, Rubenstein JL, Goebbels S, Nave KA, During M, Klugmann M, Wölfel B, Dodt HU, Zieglgänsberger W, Wotjak CT, et al. (2006) The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51:455-466. CrossRef Medline
38. Morris G., Arkadir D, Nevet A, Vaadia E, BergmanH (2004) Coincident but distinct messages of midbrain dopamine and striatal tonically active neurons. Neuron 43:133-143. CrossRef Medline
39. Nagayama S., Enerva A, Fletcher ML, Masurkar AV, Igarashi KM, Mori K, Chen W. R (2010) Differential axonal projection of mitral and tufted cells in the mouse main olfactory system. Front Neural Circuits 4:pii:120. CrossRef Medline
40. Nelson A. B, Hammack N, Yang CF, Shah NM, Seal RP, Kreitzer AC (2014) Striatal cholinergic interneurons drive GABA release from dopamine terminals. Neuron 82:63-70. CrossRef Medline
41. Neve K. A, Seamans JK, Trantham-Davidson H (2004) Dopamine receptor signaling. J Recept Signal Transduct Res 24:165-205. CrossRef Medline
42. Pakhotin P., Bracci E (2007) Cholinergic interneurons control the excitatory input to the striatum. J Neurosci 27:391-400. CrossRef Medline
43. Parlato R., Rieker C, Turiault M, Tronche F, Schütz G (2006) Survival of DA neurons is independent of CREM upregulation in absence of CREB. Genesis 44:454-464. CrossRef Medline
44. Price J. L (1973) An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. J Comp Neurol 150:87-108. CrossRef Medline
45. Robinson D. L, Venton BJ, Heien ML, Wightman RM (2003) Detecting subsecond dopamine release with fast-scan cyclic voltammetry in vivo. Clin Chem 49:1763-1773. CrossRef Medline
46. Roeper J. (2013) Dissecting the diversity of midbrain dopamine neurons. Trends Neurosci 36:336-342. CrossRef Medline
47. Schultz W. (1986) Responses of midbrain dopamine neurons to behavioral trigger stimuli in the monkey. J Neurophysiol 56:1439-1461. Medline
48. Schulz J. M, Reynolds JN (2013) Pause and rebound: sensory control of cholinergic signaling in the striatum. Trends Neurosci 36:41-50. CrossRef Medline
49. Schwob J. E, Price JL (1984) The development of lamination of afferent fibers to the olfactory cortex in rats, with additional observations in the adult. J Comp Neurol 223:203-222. CrossRef Medline
50. Sosulski D. L, Bloom ML, Cutforth T, Axel R, Datta SR (2011) Distinct representations of olfactory information in different cortical centres. Nature 472:213-216. CrossRef Medline
51. Stuber G. D, Hnasko TS, Britt JP, Edwards RH, Bonci A (2010) Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J Neurosci 30:8229-8233. CrossRef Medline
52. Tecuapetla F., Patel JC, Xenias H, English D, Tadros I, Shah F, Berlin J, Deisseroth K, Rice ME, Tepper JM, Koos T (2010) Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens. J Neurosci 30:7105-7110. CrossRef Medline
53. Tritsch N. X, Ding JB, Sabatini BL (2012) Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 490:262-266. CrossRef Medline
54. Wahle P., Meyer G (1986) The olfactory tubercle of the cat. II. Immunohistochemical compartmentation. Exp Brain Res 62:528-540. Medline
55. Wesson D. W, Wilson DA (2010) Smelling sounds: olfactory-auditory sensory convergence in the olfactory tubercle. J Neurosci 30:3013-3021. CrossRef Medline
56. Wichterle H., Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128:3759-3771. Medline
57. Witten I. B, Lin SC, Brodsky M, Prakash R, Diester I, Anikeeva P, Gradinaru V, Ramakrishnan C., Deisseroth K (2010) Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330:1677-1681. CrossRef Medline
58. Yamaguchi T., Wang HL, MoralesM (2013) Glutamate neurons in the substantia nigra compacta and retrorubral field. Eur J Neurosci 38:3602-3610. CrossRef Medline
59. Yan Z., Surmeier DJ (1997) D5 dopamine receptors enhance Zn2+-sensitive GABA(A) currents in striatal cholinergic interneurons through a PKA/PP1 cascade. Neuron 19:1115-1126. CrossRef Medline
60. Yan Z., Song WJ, Surmeier J (1997) D2 dopamine receptors reduce N-type Ca2+ currents in rat neostriatal cholinergic interneurons through a membrane-delimited, protein-kinase-C-insensitive pathway. J Neurophysiol 77:1003-1015. Medline
61. Zelano C., Bensafi M, Porter J, Mainland J, Johnson B, Bremner E, Telles C, Khan R., Sobel N (2005) Attentional modulation in human primary olfactory cortex. Nat Neurosci 8:114-120. CrossRef Medline