A glutamatergic reward input from the dorsal raphe to ventral tegmental area dopamine neurons

Nature Communications

Volumn 5, Issue , 2014, Pages

  Qi, Jia ^a   Zhang, Shiliang ^a   Wang, Hui Ling ^a   Wang, Huikun ^b   De Jesus Aceves Buendia, Jose ^a   Hoffman, Alexander F ^b   Lupica, Carl R ^b   Seal, Rebecca P ^c   Morales, Marisela ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; VESICULAR GLUTAMATE TRANSPORTER 3; AMINO ACID TRANSPORTER; VESICULAR GLUTAMATE TRANSPORTER; VESICULAR GLUTAMATE TRANSPORTER 3, MOUSE; VGLUT3 PROTEIN, RAT;

AMINO ACID; NEUROLOGY; PHENOTYPE; SIGNALING;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEPTH STIMULATION; CELL ACTIVATION; COMPARATIVE STUDY; CONTROLLED STUDY; DENDRITE; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DORSAL RAPHE NUCLEUS; ELECTRON MICROSCOPY; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; FLUORESCENCE MICROSCOPY; HYPERPOLARIZATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTRACELLULAR RECORDING; MALE; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE ENDING; NONHUMAN; NUCLEUS ACCUMBENS; OPTOGENETICS; PHENOTYPE; PHOTOSTIMULATION; PLACE PREFERENCE; POSTSYNAPTIC MEMBRANE; RAT; REWARD; SEROTONINERGIC NERVE CELL; SIGNAL TRANSDUCTION; STRIA TERMINALIS; VENTRAL TEGMENTUM; ANIMAL; C57BL MOUSE; CONDITIONED REFLEX; NERVE TRACT; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT;

AMINO ACID TRANSPORT SYSTEMS, ACIDIC; ANIMALS; CONDITIONING, CLASSICAL; DOPAMINERGIC NEURONS; DORSAL RAPHE NUCLEUS; MALE; MICE, INBRED C57BL; NEURAL PATHWAYS; OPTOGENETICS; RATS; RATS, SPRAGUE-DAWLEY; REWARD; VENTRAL TEGMENTAL AREA; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

EID: 84922552461     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6390     Document Type: Article

References (58)

1. Simon, H., Le Moal, M. & Cardo, B. Intracranial self-stimulation from the dorsal raphe nucleus of the rat: effects of the injection of parachlorophenylalanine and of alpha-methylparatyrosine. Behav. Biol. 16, 353-364 (1976).
2. Wise, R. A. & Rompre, P. P. Brain dopamine and reward. Annu. Rev. Psychol. 40, 191-225 (1989).
3. Boye, S. M. & Rompre, P. P. Mesencephalic substrate of reward: axonal connections. J. Neurosci. 16, 3511-3520 (1996).
4. Geisler, S., Derst, C., Veh, R. W. & Zahm, D. S. Glutamatergic afferents of the ventral tegmental area in the rat. J. Neurosci. 27, 5730-5743 (2007).
5. Schultz, W., Apicella, P. & Ljungberg, T. Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J. Neurosci. 13, 900-913 (1993).
6. Grace, A. A., Floresco, S. B., Goto, Y. & Lodge, D. J. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci. 30, 220-227 (2007).
7. Bobillier, P. et al. The raphe nuclei of the cat brain stem: a topographical atlas of their efferent projections as revealed by autoradiography. Brain Res. 113, 449-486 (1976).
8. Pierce, E. T., Foote, W. E. & Hobson, J. A. The efferent connection of the nucleus raphe dorsalis. Brain Res. 107, 137-144 (1976).
9. Herve, D., Pickel, V. M., Joh, T. H. & Beaudet, A. Serotonin axon terminals in the ventral tegmental area of the rat: fine structure and synaptic input to dopaminergic neurons. Brain Res. 435, 71-83 (1987).
10. Van Bockstaele, E. J., Cestari, D. M. & Pickel, V. M. Synaptic structure and connectivity of serotonin terminals in the ventral tegmental area: potential sites for modulation of mesolimbic dopamine neurons. Brain Res. 647, 307-322 (1994).
11. Hioki, H. et al. Vesicular glutamate transporter 3-expressing nonserotonergic projection neurons constitute a subregion in the rat midbrain raphe nuclei. J. Comp. Neurol. 518, 668-686 (2010).
12. Kawano, M. et al. Particular subpopulations of midbrain and hypothalamic dopamine neurons express vesicular glutamate transporter 2 in the rat brain. J. Comp. Neurol. 498, 581-592 (2006).
13. Yamaguchi, T., Wang, H. L., Li, X., Ng, T. H. & Morales, M. Mesocorticolimbic glutamatergic pathway. J. Neurosci. 31, 8476-8490 (2011).
14. Gras, C. et al. A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J. Neurosci. 22, 5442-5451 (2002).
15. Fremeau, Jr. R. T. et al. The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc. Natl Acad. Sci. USA 99, 14488-14493 (2002).
16. Schafer, M. K., Varoqui, H., Defamie, N., Weihe, E. & Erickson, J. D. Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. J. Biol. Chem. 277, 50734-50748 (2002).
17. Olds, J. & Milner, P. Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J. Comp. Physiol. Psychol. 47, 419-427 (1954).
18. Bielajew, C., Bushnik, T., Konkle, A. T. & Schindler, D. The substrate for brainstimulation reward in the lateral preoptic area. II. Connections to the ventral tegmental area. Brain Res. 881, 112-120 (2000).
19. Shizgal, P., Bielajew, C., Corbett, D., Skelton, R. & Yeomans, J. Behavioral methods for inferring anatomical linkage between rewarding brain stimulation sites. J. Comp. Physiol. Psychol. 94, 227-237 (1980).
20. Bielajew, C. & Shizgal, P. Evidence implicating descending fibers in selfstimulation of the medial forebrain bundle. J. Neurosci. 6, 919-929 (1986).
21. Anden, N. E., Dahlstrom, A., Fuxe, K. & Larsson, K. Mapping out of catecholamine and 5-hydroxytryptamine neurons innervating the telencephalon and diencephalon. Life Sci. 4, 1275-1279 (1965).
22. Calizo, L. H. et al. Raphe serotonin neurons are not homogenous: electrophysiological, morphological and neurochemical evidence. Neuropharmacology 61, 524-543 (2011).
23. Hale, M. W. & Lowry, C. A. Functional topography of midbrain and pontine serotonergic systems: implications for synaptic regulation of serotonergic circuits. Psychopharmacology (Berl) 213, 243-264 (2011).
24. Kiyasova, V. et al. A genetically defined morphologically and functionally unique subset of 5-HT neurons in the mouse raphe nuclei. J. Neurosci. 31, 2756-2768 (2011).
25. Bang, S. J., Jensen, P. & Dymecki, S. M. Commons KG. Projections and interconnections of genetically defined serotonin neurons in mice. Eur. J. Neurosci. 35, 85-96 (2012).
26. Boureau, Y. L. & Dayan, P. Opponency revisited: competition and cooperation between dopamine and serotonin. Neuropsychopharmacology 36, 74-97 (2011).
27. Cools, R., Nakamura, K. & Daw, N. D. Serotonin and dopamine: unifying affective, activational, and decision functions. Neuropsychopharmacology 36, 98-113 (2011).
28. Hayes, D. J. & Greenshaw, A. J. 5-HT receptors and reward-related behaviour: a review. Neurosci. Biobehav. Rev. 35, 1419-1449 (2011).
29. Kranz, G. S., Kasper, S. & Lanzenberger, R. Reward and the serotonergic system. Neuroscience 166, 1023-1035 (2010).
30. Phillips, A. G., Carter, D. A. & Fibiger, H. C. Differential effects of parachlorophenylalanine on self-stimulation in caudate-putamen and lateral hypothalamus. Psychopharmacology (Berl) 49, 23-27 (1976).
31. Poschel, B. P. & Ninteman, F. W. Intracranial reward and the forebrain's serotonergic mechanism: studies employing para-chlorophenylalanine and para-chloroamphetamine. Physiol. Behav. 7, 39-46 (1971).
32. Poschel, B. P., Ninteman, F. W., McLean, J. R. & Potoczak, D. Intracranial reward after 5,6-dihydroxytryptamine: further evidence for serotonin's inhibitory role. Life Sci. 15, 1515-1522 (1974).
33. Fletcher, P. J., Tampakeras, M. & Yeomans, J. S. Median raphe injections of 8-OH-DPAT lower frequency thresholds for lateral hypothalamic selfstimulation. Pharmacol. Biochem. Behav. 52, 65-71 (1995).
34. Fletcher, P. J., Ming, Z. H. & Higgins, G. A. Conditioned place preference induced by microinjection of 8-OH-DPAT into the dorsal or median raphe nucleus. Psychopharmacology (Berl) 113, 31-36 (1993).
35. Liu, Z. H. & Ikemoto, S. The midbrain raphe nuclei mediate primary reinforcement via GABA(A) receptors. Eur. J. Neurosci. 25, 735-743 (2007).
36. Shin, R. & Ikemoto, S. The GABAB receptor agonist baclofen administered into the median and dorsal raphe nuclei is rewarding as shown by intracranial selfadministration and conditioned place preference in rats. Psychopharmacology (Berl) 208, 545-554 (2010).
37. Redgrave, P. & Horrell, R. I. Potentiation of central reward by localised perfusion of acetylcholine and 5-hydroxytryptamine. Nature 262, 305-307 (1976).
38. Liu, Z. et al. Dorsal raphe neurons signal reward through 5-HT and Glutamate. Neuron 81, 1360-1374 (2014).
39. Schultz, W., Dayan, P. & Montague, P. R. A neural substrate of prediction and reward. Science 275, 1593-1599 (1997).
40. Bromberg-Martin, E. S., Hikosaka, O. & Nakamura, K. Coding of task reward value in the dorsal raphe nucleus. J. Neurosci. 30, 6262-6272 (2010).
41. Nakamura, K., Matsumoto, M. & Hikosaka, O. Reward-dependent modulation of neuronal activity in the primate dorsal raphe nucleus. J. Neurosci. 28, 5331-5343 (2008).
42. Miyazaki, K. W., Miyazaki, K. & Doya, K. Activation of the central serotonergic system in response to delayed but not omitted rewards. Eur. J. Neurosci. 33, 153-160 (2011).
43. Ranade, S. P. & Mainen, Z. F. Transient firing of dorsal raphe neurons encodes diverse and specific sensory, motor, and reward events. J. Neurophysiol. 102, 3026-3037 (2009).
44. Sesack, S. R. & Pickel, V. M. Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J. Comp. Neurol. 320, 145-160 (1992).
45. Omelchenko, N. & Sesack, S. R. Glutamate synaptic inputs to ventral tegmental area neurons in the rat derive primarily from subcortical sources. Neuroscience 146, 1259-1274 (2007).
46. Omelchenko, N. & Sesack, S. R. Periaqueductal gray afferents synapse onto dopamine and GABA neurons in the rat ventral tegmental area. J. Neurosci. Res. 88, 981-991 (2010).
47. Omelchenko, N., Bell, R. & Sesack, S. R. Lateral habenula projections to dopamine and GABA neurons in the rat ventral tegmental area. Eur. J. Neurosci. 30, 1239-1250 (2009).
48. Clements, J. R. & Grant, S. Glutamate-like immunoreactivity in neurons of the laterodorsal tegmental and pedunculopontine nuclei in the rat. Neurosci. Lett. 120, 70-73 (1990).
49. Charara, A., Smith, Y. & Parent, A. Glutamatergic inputs from the pedunculopontine nucleus to midbrain dopaminergic neurons in primates: Phaseolus vulgaris-leucoagglutinin anterograde labeling combined with postembedding glutamate and GABA immunohistochemistry. J. Comp. Neurol. 364, 254-266 (1996).
50. Lammel, S. et al. Input-specific control of reward and aversion in the ventral tegmental area. Nature 491, 212-217 (2012).
51. Grimes, W. N., Seal, R. P., Oesch, N., Edwards, R. H. & Diamond, J. S. Genetic targeting and physiological features of VGLUT3 amacrine cells. Vis. Neurosci. 28, 381-392 (2011).
52. Yamaguchi, T., Sheen, W. & Morales, M. Glutamatergic neurons are present in the rat ventral tegmental area. Eur. J. Neurosci. 25, 106-118 (2007).
53. Boulland, J. L. et al. Vesicular glutamate and GABA transporters sort to distinct sets of vesicles in a population of presynaptic terminals. Cereb. Cortex 19, 241-248 (2009).
54. Tagliaferro, P. & Morales, M. Synapses between corticotropin-releasing factor-containing axon terminals and dopaminergic neurons in the ventral tegmental area are predominantly glutamatergic. J. Comp. Neurol. 506, 616-626 (2008).
55. Bjijou, Y., Stinus, L., Le Moal, M. & Cador, M. Evidence for selective involvement of dopamine D1 receptors of the ventral tegmental area in the behavioral sensitization induced by intra-ventral tegmental area injections of D-amphetamine. J. Pharmacol. Exp. Ther. 277, 1177-1187 (1996).
56. Peters, A., Palay, S. L. & Webster, H. d. The Fine Structure of the Nervous System: Neurons and Their Supporting Cells (Oxford Univ. Press, 1991).
57. Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates (Elsevier, 2007).
58. Paxinos, G. & Franklin, K. B. J. The Mouse Brain in Stereotaxic Coordinates (Academic, 2001).