Association with reward negatively modulates short latency phasic conditioned responses of dorsal raphe nucleus neurons inr feely moving rats

Journal of Neuroscience

Volumn 33, Issue 11, 2013, Pages 5065-5078

  Li, Yuhong ^a   Dalphin, Neil ^a   Hyland, Brian I ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; BRAIN ELECTROPHYSIOLOGY; COMPARATIVE STUDY; DOPAMINERGIC NERVE CELL; DORSAL RAPHE NUCLEUS; HISTOLOGY; LATENT PERIOD; LICKING; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; RAT; TASK PERFORMANCE;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; ACTION POTENTIALS; ANIMALS; APOMORPHINE; CONDITIONING (PSYCHOLOGY); CUES; DOPAMINE AGONISTS; MALE; NEURONS; RAPHE NUCLEI; RATS; RATS, WISTAR; REACTION TIME; REWARD; SEROTONIN RECEPTOR AGONISTS; WAKEFULNESS;

EID: 84874872651     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5679-12.2013     Document Type: Article

References (81)

1. Abrams JK, Johnson PL, Hollis JH, Lowry CA (2004) Anatomic and functional topography of the dorsal raphe nucleus. Ann N Y Acad Sci 1018: 46-57. CrossRef Medline
2. Aebischer P, Schultz W (1984) The activity of pars compacta neurons of the monkey substantia nigra is depressed by apomorphine. Neurosci Lett 50:25-29. CrossRef Medline
3. Aghajanian GK, Bunney BS (1977) Dopamine "autoreceptors": pharmacological characterization by microiontophoretic single cell recording studies. Naunyn-Schmiedeberg's Arch Pharmacol 297:1-7. CrossRef Medline
4. Alex KD, Pehek EA (2007) Pharmacologic mechanisms of serotonergic regulation of dopamine neurotransmission. Pharmacol Ther 113:296-320. CrossRef Medline
5. Allers KA, Sharp T (2003) Neurochemical and anatomical identification of fast-and slow-firing neurones in the rat dorsal raphe nucleus using juxtacellular labelling methods in vivo. Neuroscience 122:193-204. CrossRef Medline
6. Beck SG, Pan YZ, Akanwa AC, Kirby LG (2004) Median and dorsal raphe neurons are not electrophysiologically identical. J Neurophysiol 91:994-1005. CrossRef Medline
7. Bromberg-Martin ES, Hikosaka O, Nakamura K (2010) Coding of task reward value in the dorsal raphe nucleus. J Neurosci 30:6262-6272. CrossRef Medline
8. Bubar MJ, Cunningham KA (2007) Distribution of serotonin 5-HT2C receptors in the ventral tegmental area. Neuroscience 146:286-297. CrossRef Medline
9. Bunney BS, Walters JR, Roth RH, Aghajanian GK (1973) Dopaminergic neurons: effect of antipsychotic drugs and amphetamine on single cell activity. J Pharmacol Exp Ther 185:560-571. Medline
10. Calizo LH, Akanwa A, Ma X, Pan YZ, Lemos JC, Craige C, Heemstra LA, Beck SG (2011) Raphe serotonin neurons are not homogenous: electrophysiological, morphological and neurochemical evidence. Neuropharmacology 61:524-543. CrossRef Medline
11. Cardinal RN (2006) Neural systems implicated in delayed and probabilistic reinforcement. Neural Netw 19:1277-1301. CrossRef Medline
12. Cools R, Roberts AC, Robbins TW (2008) Serotoninergic regulation of emotional and behavioural control processes. Trends Cogn Sci 12:31-40. CrossRef Medline
13. Daw ND, Kakade S, Dayan P (2002) Opponent interactions between serotonin and dopamine. Neural Netw 15:603-616. CrossRef Medline
14. Dayan P, Huys QJ (2009) Serotonin in affective control. Annu Rev Neurosci 32:95-126. CrossRef Medline
15. Dayan P, Huys QJ (2008) Serotonin, inhibition, and negative mood. PLo S Comput Biol 4:e4. CrossRef Medline
16. Deakin JF, Graeff FG (1991) 5-HT and mechanisms of defence. J Psychopharmacol 5:305-315. CrossRef Medline
17. Descarries L, Watkins KC, Garcia S, Beaudet A (1982) The serotonin neurons in nucleus raphe dorsalis of adult rat: a light and electron microscope radioautographic study. J Comp Neurol 207:239-254. CrossRef Medline
18. Doya K (2002) Metalearning and neuromodulation. Neural Netw 15:495-506. CrossRef Medline
19. Dremencov E, El Mansari M, Blier P (2009) Effects of sustained serotonin reuptake inhibition on the firing of dopamine neurons in the rat ventral tegmental area. J Psychiatry Neurosci 34:223-229. Medline
20. Evenden JL (1999) Varieties of impulsivity. Psychopharmacology 146:348-361. CrossRef Medline
21. Ferrante M, Migliore M, Ascoli GA (2009) Feed-forward inhibition as a buffer of the neuronal input-output relation. Proc Natl Acad Sci U S A 106:18004-18009. CrossRef Medline
22. Fornal CA, Litto WJ, Metzler CW, Marrosu F, Tada K, Jacobs BL (1994) Single-unit responses of serotonergic dorsal raphe neurons to 5-HT1A agonist and antagonist drug administration in behaving cats. J Pharmacol Exp Ther 270:1345-1358. CrossRef Medline
23. Fornal CA, Metzler CW, Marrosu F, Ribiero-do-Valle LE, Jacobs BL (1996) A subgroup of dorsal raphe serotonergic neurons in the cat is strongly activated during oral-buccal movements. Brain Res 716:123-133. CrossRef Medline
24. Gervais J, Rouillard C (2000) Dorsal raphe stimulation differentially modulates dopaminergic neurons in the ventral tegmental area and substantia nigra. Synapse 35:281-291. CrossRef Medline
25. Grace AA, Bunney BS (1980) Nigral dopamine neurons: intracellular recording and identification with L-dopa injection and histofluorescence. Science 210:654-656. CrossRef Medline
26. Guiard BP, El Mansari M, Merali Z, Blier P (2008) Functional interactions between dopamine, serotonin and norepinephrine neurons: an in-vivo electrophysiological study in rats with monoaminergic lesions. Int J Neuropsychopharmacol 11:625-639. CrossRef Medline
27. Hajós M, Gartside SE, Villa AE, Sharp T (1995) Evidence for a repetitive (burst) firing pattern in a sub-population of 5-hydroxytryptamine neurons in the dorsal and median raphe nuclei of the rat. Neuroscience 69: 189-197. CrossRef Medline
28. Hajós M, Allers KA, Jennings K, Sharp T, Charette G, Sík A, Kocsis B (2007) Neurochemical identification of stereotypic burst-firing neurons in the rat dorsal raphe nucleus using juxtacellular labelling methods. Eur J Neurosci 25:119-126. CrossRef Medline
29. Hale MW, Lowry CA (2011) Functional topography of midbrain and pontine serotonergic systems: implications for synaptic regulation of serotonergic circuits. Psychopharmacology 213:243-264. CrossRef Medline
30. Hattox A, Li Y, Keller A (2003) Serotonin regulates rhythmic whisking. Neuron 39:343-352. CrossRef Medline
31. Hensler JG (2006) Serotonergic modulation of the limbic system. Neurosci Biobehav Rev 30:203-214. CrossRef Medline
32. Hervé D, Pickel VM, Joh TH, Beaudet A (1987) Serotonin axon terminals in the ventral tegmental area of the rat: fine structure and synaptic input to dopaminergic neurons. Brain Res 435:71-83. CrossRef Medline
33. Heym J, Trulson ME, Jacobs BL (1982) Raphe unit activity in freely moving cats: effects of phasic auditory and visual stimuli. Brain Res 232:29-39. CrossRef Medline
34. Hyland BI, Reynolds JN, Hay J, Perk CG, Miller R (2002) Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 114:475-492. CrossRef Medline
35. Jacobs BL, Azmitia EC (1992) Structure and function of the brain serotonin system. Physiol Rev 72:165-229. Medline
36. Jacobs BL, Fornal CA (1991) Activity of brain serotonergic neurons in the behaving animal. Pharmacol Rev 43:563-578. Medline
37. Kaneoke Y, Vitek JL (1996) Burst and oscillation as disparate neuronal properties. J Neurosci Methods 68:211-223. CrossRef Medline
38. Kirby LG, Pernar L, Valentino RJ, Beck SG (2003) Distinguishing characteristics of serotonin and non-serotonin-containing cells in the dorsal raphe nucleus: electrophysiological and immunohistochemical studies. Neuroscience 116:669-683. CrossRef Medline
39. Kocsis B, Vertes RP (1992) Dorsal raphe neurons: synchronous discharge with the theta rhythm of the hippocampus in the freely behaving rat. J Neurophysiol 68:1463-1467. Medline
40. Kocsis B, Varga V, Dahan L, Sik A (2006) Serotonergic neuron diversity: identification of raphe neurons with discharges time-locked to the hippocampal theta rhythm. Proc Natl Acad Sci U S A 103:1059-1064. CrossRef Medline
41. Kranz GS, Kasper S, Lanzenberger R (2010) Reward and the serotonergic system. Neuroscience 166:1023-1035. CrossRef Medline
42. Ljungberg T, Apicella P, Schultz W (1992) Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 67:145-163. Medline
43. Lowry CA, Hale MW, Evans AK, Heerkens J, Staub DR, Gasser PJ, Shekhar A (2008) Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus. Ann N Y Acad Sci 1148:86-94. CrossRef Medline
44. 2 receptor inhibition. J Neurosci 28:8908-8913. CrossRef Medline
45. Marinelli S, Schnell SA, Hack SP, Christie MJ, Wessendorf MW, Vaughan CW (2004) Serotonergic and nonserotonergic dorsal raphe neurons are pharmacologically and electrophysiologically heterogeneous. J Neurophysiol 92:3532-3537. CrossRef Medline
46. Michelsen KA, Schmitz C, Steinbusch HW (2007) The dorsal raphe nucleus-from silver stainings to a role in depression. Brain Res Rev 55: 329-342. CrossRef Medline
47. Mirenowicz J, Schultz W (1996) Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 379:449-451. CrossRef Medline
48. Miyazaki K, Miyazaki KW, Doya K (2011a) Activation of dorsal raphe serotonin neurons underlies waiting for delayed rewards. J Neurosci 31:469-479. CrossRef Medline
49. Miyazaki KW, Miyazaki K, Doya K (2011b) Activation of the central serotonergic system in response to delayed but not omitted rewards. Eur J Neurosci 33:153-160. CrossRef Medline
50. Miyazaki KW, Miyazaki K, Doya K (2012) Activation of dorsal raphe serotonin neurons is necessary for waiting for delayed rewards. J Neurosci 32:10451-10457. CrossRef Medline
51. Montagne-Clavel J, Oliveras JL, Martin G (1995) Single-unit recordings at dorsal raphe nucleus in the awake-anesthetized rat: spontaneous activity and responses to cutaneous innocuous and noxious stimulations. Pain 60:303-310. CrossRef Medline
52. Monti JM (2010) The structure of the dorsal raphe nucleus and its relevance to the regulation of sleep and wakefulness. Sleep Med Rev 14:307-317. CrossRef Medline
53. Motulsky HJ, Brown RE (2006) Detecting outliers when fitting data with nonlinear regression-a new method based on robust nonlinear regression and the false discovery rate. BMC Bioinformatics 7:123. CrossRef Medline
54. Nakahama H, Shima K, Yamamoto M, Aya K (1981) Regularity of the spontaneous discharge of neurons in the nucleus raphe dorsalis of the cat. Neurosci Lett 23:161-165. CrossRef Medline
55. Nakamura K, Matsumoto M, Hikosaka O (2008) Reward-dependent modulation of neuronal activity in the primate dorsal raphe nucleus. J Neurosci 28:5331-5343. CrossRef Medline
56. Nedergaard S, Bolam JP, Greenfield SA (1988) Facilitation of a dendritic calcium conductance by 5-hydroxytryptamine in the substantia nigra. Nature 333:174-177. CrossRef Medline
57. Pan WX, Schmidt R, Wickens JR, Hyland BI (2005) Dopamine cells respond to predicted events during classical conditioning: evidence for eligibility traces in the reward-learning network. J Neurosci 25:6235-6242. CrossRef Medline
58. Pan WX, Schmidt R, Wickens JR, Hyland BI (2008) Tripartite mechanism of extinction suggested by dopamine neuron activity and temporal difference model. J Neurosci 28:9619-9631. CrossRef Medline
59. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, Ed 3. London: Academic.
60. Quirk GJ, Repa C, LeDoux JE (1995) Fear conditioning enhances shortlatency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron 15:1029-1039. CrossRef Medline
61. Ranade SP, Mainen ZF (2009) Transient firing of dorsal raphe neurons encodes diverse and specific sensory, motor, and reward events. J Neurophysiol 102:3026-3037. CrossRef Medline
62. Rasmussen K, Strecker RE, Jacobs BL (1986) Single unit response of noradrenergic, serotonergic and dopaminergic neurons in freely moving cats to simple sensory stimuli. Brain Res 369:336-340. CrossRef Medline
63. Rogawski MA, Aghajanian GK (1980) Norepinephrine and serotonin: opposite effects on the activity of lateral geniculate neurons evoked by optic pathway stimulation. Exp Neurol 69:678-694. CrossRef Medline
64. Sakai K, Crochet S (2001) Differentiation of presumed serotonergic dorsal raphe neurons in relation to behavior and wake-sleep states. Neuroscience 104:1141-1155. CrossRef Medline
65. Schmidt BJ, Jordan LM (2000) The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull 53:689-710. CrossRef Medline
66. Schultz W, Dickinson A (2000) Neuronal coding of prediction errors. Annu Rev Neurosci 23:473-500. CrossRef Medline
67. Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593-1599. CrossRef Medline
68. Schweimer JV, Ungless MA (2010) Phasic responses in dorsal raphe serotonin neurons to noxious stimuli. Neuroscience 171:1209-1215. CrossRef Medline
69. Soubrie P (1986) Reconciling the role of central serotonin neurons in human and animal behavior. Behav Brain Sci 9:319-335. CrossRef
70. Sprouse JS, Aghajanian GK (1987) Electrophysiological responses of serotoninergic dorsal raphe neurons to 5-HT1A and 5-HT1B agonists. Synapse 1:3-9. CrossRef Medline
71. Stratford TR, Wirtshafter D (1990) Ascending dopaminergic projections from the dorsal raphe nucleus in the rat. Brain Res 511:173-176. CrossRef Medline
72. Tobler PN, Dickinson A, Schultz W (2003) Coding of predicted reward omission by dopamine neurons in a conditioned inhibition paradigm. J Neurosci 23:10402-10410. Medline
73. Vandermaelen CP, Aghajanian GK (1983) Electrophysiological and pharmacological characterization of serotonergic dorsal raphe neurons recorded extracellularly and intracellularly in rat brain slices. Brain Res 289:109-119. CrossRef Medline
74. Waelti P, Dickinson A, Schultz W (2001) Dopamine responses comply with basic assumptions of formal learning theory. Nature 412:43-48. CrossRef Medline
75. Watabe-Uchida M, Zhu L, Ogawa SK, Vamanrao A, Uchida N (2012) Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 74:858-873. CrossRef Medline
76. Waterhouse BD, Moises HC, Woodward DJ (1986) Interaction of serotonin with somatosensory cortical neuronal responses to afferent synaptic inputs and putative neurotransmitters. Brain Res Bull 17:507-518. CrossRef Medline
77. Waterhouse BD, Azizi SA, Burne RA, Woodward DJ (1990) Modulation of rat cortical area 17 neuronal responses to moving visual stimuli during norepinephrine and serotonin microiontophoresis. Brain Res 514:276-292. CrossRef Medline
78. Waterhouse BD, Devilbiss D, Seiple S, Markowitz R (2004) Sensorimotor-related discharge of simultaneously recorded, single neurons in the dorsal raphe nucleus of the awake, unrestrained rat. Brain Res 1000:183-191. CrossRef Medline
79. Wilson CJ, Groves PM (1981) Spontaneous firing patterns of identified spiny neurons in the rat neostriatum. Brain Res 220:67-80. CrossRef Medline
80. Winstanley CA, Theobald DE, Dalley JW, Cardinal RN, Robbins TW (2006) Double dissociation between serotonergic and dopaminergic modulation of medial prefrontal and orbitofrontal cortex during a test of impulsive choice. Cereb Cortex 16:106-114. CrossRef Medline
81. Witten IB, Steinberg EE, Lee SY, Davidson TJ, Zalocusky KA, Brodsky M, Yizhar O, Cho SL, Gong S, Ramakrishnan C, Stuber GD, Tye KM, Janak PH, Deisseroth K (2011) Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 72:721-733. CrossRef Medline