Sources of input to the rostromedial tegmental nucleus, ventral tegmental area, and lateral habenula compared: A study in rat

Journal of Comparative Neurology

Volumn 523, Issue 16, 2015, Pages 2426-2456

  Yetnikoff, Leora ^a,b   Cheng, Anita Y ^a   Lavezzi, Heather N ^a   Parsley, Kenneth P ^a   Zahm, Daniel S ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

Inhibitory control; Lateral habenula; Rostromedial tegmental nucleus

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN MAPPING; BRAIN SIZE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ENTOPEDUNCULAR NUCLEUS; HABENULA; MALE; MOTOR PERFORMANCE; NERVE CELL NETWORK; NERVE FIBER; NERVE PROJECTION; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; RAT; ROSTROMEDIAL TEGMENTAL NUCLEUS; SUPERIOR COLLICULUS; TEGMENTUM; VENTRAL TEGMENTUM; ANATOMY AND HISTOLOGY; ANIMAL; COMPARATIVE STUDY; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; MICROPHOTOGRAPHY; NERVE CELL; NERVE TRACT; NEUROANATOMICAL TRACT TRACING; SPRAGUE DAWLEY RAT;

ANIMALS; FLUORESCENT ANTIBODY TECHNIQUE; HABENULA; MALE; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEURONS; PHOTOMICROGRAPHY; RATS, SPRAGUE-DAWLEY; TEGMENTUM MESENCEPHALI;

EID: 84941997330     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23797     Document Type: Article

References (153)

1. Alheid GF, Heimer L. 1988. New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27:1-39.
2. Araki M, McGeer PL, Kimura H. 1988. The efferent projections of the rat lateral habenular nucleus revealed by the PHA-L anterograde tracing method. Brain Res 441:319-330.
3. Arts MP, Cools AR. 1998. Bilateral 6-hydroxydopamine lesion in the dopaminergic A8 cell group produces long-lasting deficits in motor programming of cats. Behav Neurosci 112:102-115.
4. Arts MP, Cools AR. 1999. 6-hydroxydopamine lesion in the A8 cell group of cats produces a short-lasting decreased accuracy in goal-directed forepaw-movements. Behav Brain Res 103:13-21.
5. Arts MP, Cools AR. 2000. D1 and D2 dopamine receptor agonists improve deficits in motor programming of cats with a 6-hydroxydopamine lesion in the A8 cell group. Behav Brain Res 108:73-84.
6. Arts MP, Bemelmans FF, Cools AR. 1998. Role of the retrorubral nucleus in striatally elicited orofacial dyskinesia in cats: effects of muscimol and bicuculline. Psychopharmacology (Berl) 140:150-156.
7. Austin MC, Kalivas PW. 1989. Blockade of enkephalinergic and GABAergic mediated locomotion in the nucleus accumbens by muscimol in the ventral pallidum. Jpn J Pharmacol 50:487-490.
8. Austin MC, Kalivas PW. 1990. Enkephalinergic and GABAergic modulation of motor activity in the ventral pallidum. J Pharmacol Exp Ther 252:1370-1377.
9. Austin MC, Kalivas PW. 1991. Dopaminergic involvement in locomotion elicited from the ventral pallidum/substantia innominata. Brain Res 542:123-131.
10. Balcita-Pedicino JJ, Omelchenko N, Bell, R, Sesack SR. 2011. The inhibitory influence of the lateral habenula on midbrain dopamine cells: ultrastructural evidence for indirect mediation via the rostromedial mesopontine tegmental nucleus. J Comp Neurol 519:1143-1164.
11. Barrot M. 2014. The ventral tegmentum and dopamine: a new wave of diversity. Neuroscience 282C:243-247.
12. Barrot M, Thome J. 2011. Discovering a new anatomical structure in the brain: implications for neuropsychiatry and therapy. World J Biol Psychiatry 12(Suppl 1):19-22.
13. Bentivoglio M, Morelli M. 2005. The organization and circuits of mesencephalic dopaminergic neurons and the distribution of dopamine receptors in the brain. In: Dunnett SB, Bentivoglio M, Björkland A, Hökfelt T, editors. Handbook of chemical neuroanatomy: dopamine (vol. 21). Amsterdam: Elsevier. p 1-107.
14. Bernard R, Veh RW. 2012. Individual neurons in the rat lateral habenular complex project mostly to the dopaminergic ventral tegmental area or to the serotonergic raphe nuclei. J Comp Neurol 520:2545-2558.
15. Berridge KC. 2007. The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology 191:391-431.
16. Björklund A, Dunnett SB. 2007. Dopamine neuron systems in the brain: an update. Trends Neurosci 30:194-202.
17. Bourdy R, Barrot M. 2012. A new control center for dopaminergic systems: pulling the VTA by the tail. Trends Neurosci 35:681-690.
18. Bourdy R, Sanchez-Catalan MJ, Kaufling J, Balcita-Pedicino JJ, Freund-Mercier MJ, Veinante, P, Sesack SR, Georges F, Barrot M. 2014. Control of the nigrostriatal dopamine neuron activity and motor function by the tail of the ventral tegmental area. Neuropsychopharmacology 39:2788-2798.
19. Brinschwitz K, Dittgen A, Madai VI, Lommel R, Geisler S, Veh RW. 2010. Glutamatergic axons from the lateral habenula mainly terminate on GABAergic neurons of the ventral midbrain. Neuroscience 168:463-476.
20. Bromberg-Martin ES, Matsumoto M, Hikosaka O. 2010. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68:815-834.
21. Brown PL, Shepard PD. 2013. Lesions of the fasciculus retroflexus alter footshock-induced cFos expression in the mesopontine rostromedial tegmental area of rats. PloS One 8:e60678.
22. Chen JC, Liang KW, Huang YK, Liang CS, Chiang YC. 2001. Significance of glutamate and dopamine neurons in the ventral pallidum in the expression of behavioral sensitization to amphetamine. Life Sci 68:973-983.
23. Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N. 2012. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482:85-88.
24. Colussi-Mas J, Geisler S, Zimmer L, Zahm DS, Berod A. 2007. Activation of afferents to the ventral tegmental area in response to acute amphetamine: a double-labelling study. Eur J Neurosci 26:1011-1025.
25. Dean P, Mitchell IJ, Redgrave P. 1988. Contralateral head movements produced by microinjection of glutamate into superior colliculus of rats: evidence for mediation by multiple output pathways. Neuroscience 24:491-500.
26. Fields HL, Hjelmstad GO, Margolis EB, Nicola SM. 2007. Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci 30:289-316.
27. Fiorillo CD, Song MR, Yun SR. 2013. Multiphasic temporal dynamics in responses of midbrain dopamine neurons to appetitive and aversive stimuli. J Neurosci 33:4710-4725.
28. Floresco SB, West AR, Ash B, Moore H, Grace AA. 2003. Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 6:968-973.
29. Geerling JC, Shin JW, Chimenti PC, Loewy AD. 2010. Paraventricular hypothalamic nucleus: axonal projections to the brainstem. J Comp Neurol 518:1460-1499.
30. Geisler, S, Trimble M. 2008. The lateral habenula: no longer neglected. CNS Spectr 13:484-489.
31. Geisler S, Zahm DS. 2005. Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions. J Comp Neurol 490:270-294.
32. Geisler S, Zahm DS. 2006. Neurotensin afferents of the ventral tegmental area in the rat: [1] re-examination of their origins and [2] responses to acute psychostimulant and antipsychotic drug administration. Eur J Neurosci 24:116-134.
33. Geisler S, Derst C, Veh RW, Zahm DS. 2007. Glutamatergic afferents of the ventral tegmental area in the rat. J Neurosci 27:5730-5743.
34. Geisler S, Marinelli M, Degarmo B, Becker ML, Freiman AJ, Beales M, Meredith GM, Zahm DS. 2008. Prominent activation of brainstem and pallidal afferents of the ventral tegmental area by cocaine. Neuropsychopharmacology 33:2688-2700.
35. Gonçalves L, Sego C, Metzger M. 2012. Differential projections from the lateral habenula to the rostromedial tegmental nucleus and ventral tegmental area in the rat. J Comp Neurol 520:1278-1300.
36. Gong W, Neill DB, Lynn M, Justice JB Jr. 1999. Dopamine D1/D2 agonists injected into nucleus accumbens and ventral pallidum differentially affect locomotor activity depending on site. Neuroscience 93:1349-1358.
37. Grace AA. 1988. In vivo and in vitro intracellular recordings from rat midbrain dopamine neurons. Ann N Y Acad Sci 537:51-76.
38. Grace AA, Floresco SB, Goto Y, Lodge DJ. 2007. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci 30:220-227.
39. Hart AS, Rutledge RB, Glimcher PW, Phillips PE. 2014. Phasic dopamine release in the rat nucleus accumbens symmetrically encodes a reward prediction error term. J Neurosci 34:698-704.
40. Heimer L, Alheid GF. 1991. Piecing together the puzzle of basal forebrain anatomy. Adv Exp Med Biol 295:1-42.
41. Heimer L, Van Hoesen GW. 2006. The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci Biobehav Rev 30:126-147.
42. Heimer L, de Olmos J, Alheid GF, Zaborszky L. 1991a. "Perestroika" in the basal forebrain: opening the border between neurology and psychiatry. Prog Brain Res 87:109-165.
43. Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C. 1991b. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41:89-125.
44. Heimer L, Van Hoesen GW, Trimble M, Zahm DS. 2008. Anatomy of neuropsychiatry. The new anatomy of the basal forebrain and its implications for neuropsychiatric illness. Amsterdam: Elsevier.
45. Hennigan K, D'Ardenne K, McClure SM. 2015. Distinct midbrain and habenula pathways are involved in processing aversive events in humans. J Neurosci 35:198-208.
46. Herkenham M, Nauta WJ. 1977. Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber-of-passage problem. J Comp Neurol 173:123-146.
47. Herkenham M, Nauta WJ. 1979. Efferent connections of the habenular nuclei in the rat. J Comp Neurol 187:19-47.
48. Hittinger M, Horn AK. 2012. The anatomical identification of saccadic omnipause neurons in the rat brainstem. Neuroscience 210:191-199.
49. Hökfelt T, Mårtensson R, Björklund A, Kleinau S, Goldstein M. 1984. Distribution maps of tyrosine-hydroxylase-immunoreactive neurons in the rat brain. In: Björklund A, Hökfelt T, editors. Classical transmitters in the CNS. Handbook of chemical neuroanatomy, vol. 2, part I. Amsterdam: Elsevier. p 277-379.
50. Hong S, Hikosaka O. 2013. Diverse sources of reward value signals in the basal ganglia nuclei transmitted to the lateral habenula in the monkey. Front Hum Neurosci 7:778.
51. Hong S, Jhou TC, Smith M, Saleem KS, Hikosaka O. 2011. Negative reward signals from the lateral habenula to dopamine neurons are mediated by rostromedial tegmental nucleus in primates. J Neurosci 31:11457-11471.
52. Hubert GW, Manvich DF, Kuhar MJ. 2010. Cocaine and amphetamine-regulated transcript-containing neurons in the nucleus accumbens project to the ventral pallidum in the rat and may inhibit cocaine-induced locomotion. Neuroscience 165:179-187.
53. Hur EE, Zaborszky L. 2005. Vglut2 afferents to the medial prefrontal and primary somatosensory cortices: a combined retrograde tracing in situ hybridization study [corrected]. J Comp Neurol 483:351-373.
54. 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.
55. Isa T, Sasaki S. 2002. Brainstem control of head movements during orienting; organization of the premotor circuits. Prog Neurobiol 66:205-241.
56. Jhou T. 2005. Neural mechanisms of freezing and passive aversive behaviors. J Comp Neurol 493:111-114.
57. Jhou TC, Fields HL, Baxter MG, Saper CB, Holland PC. 2009a. The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 61:786-800.
58. Jhou TC, Geisler S, Marinelli M, Degarmo BA, Zahm DS. 2009b. The mesopontine rostromedial tegmental nucleus: a structure targeted by the lateral habenula that projects to the ventral tegmental area of Tsai and substantia nigra compacta. J Comp Neurol 513:566-596.
59. Jhou TC, Xu SP, Lee MR, Gallen CL, Ikemoto S. 2012. Mapping of reinforcing and analgesic effects of the mu opioid agonist endomorphin-1 in the ventral midbrain of the rat. Psychopharmacology (Berl) 224:303-312.
60. Jhou TC, Good CH, Rowley CS, Xu SP, Wang H, Burnham NW, Hoffman AF, Lupica CR, Ikemoto S. 2013. Cocaine drives aversive conditioning via delayed activation of dopamine-responsive habenular and midbrain pathways. J Neurosci 33:7501-7512.
61. Ji H, Shepard PD. 2007. Lateral habenula stimulation inhibits rat midbrain dopamine neurons through a GABAA receptor-mediated mechanism. J Neurosci 27:6923-6930.
62. Jiang ZC, Pan Q, Zheng C, Deng XF, Wang JY, Luo F. 2014. Inactivation of the prelimbic rather than infralimbic cortex impairs acquisition and expression of formalin-induced conditioned place avoidance. Neurosci Lett 569:89-93.
63. Johnson PI, Napier TC. 2000. Ventral pallidal injections of a mu antagonist block the development of behavioral sensitization to systemic morphine. Synapse 38:61-70.
64. Johnson K, Churchill L, Klitenick MA, Hooks MS, Kalivas PW. 1996. Involvement of the ventral tegmental area in locomotion elicited from the nucleus accumbens or ventral pallidum. J Pharmacol Exp Ther 277:1122-1131.
65. June HL, Foster KL, McKay PF, Seyoum R, Woods JE, Harvey SC, Eiler WJ, Grey C, Carroll MR, McCane S, Jones CM, Yin W, Mason D, Cummings R, Garcia M, Ma C, Sarma PV, Cook JM, Skolnick P. 2003. The reinforcing properties of alcohol are mediated by GABA(A1) receptors in the ventral pallidum. Neuropsychopharmacology 28:2124-2137.
66. Kalivas PW, Klitenick MA, Hagler H, Austin MC. 1991. GABAergic and enkephalinergic regulation of locomotion in the ventral pallidum: involvement of the mesolimbic dopamine system. In: Napier TC, Kaliavs PW, Hanin I, editors. The basal forebrain. Anatomy to function. New York: Plenum Press (Adv Exp Med Biol 295). p 315-326.
67. Kaufling J, Veinante P, Pawlowski SA, Freund-Mercier M-J, Barrot M. 2009. Afferents to the GABAergic tail of the ventral tegmental area in the rat. J Comp Neurol 513:597-621.
68. Kelly PH, Seviour PW, Iversen SD. 1975. Amphetamine and apomorphine responses in the rat following 6-OHDA lesions of the nucleus accumbens septi and corpus striatum. Brain Res 94:507-522.
69. Kim U. 2009. Topographic commissural and descending projections of the habenula in the rat. J Comp Neurol 513:173-187.
70. Kowski AB, Geisler S, Krauss M, Veh RW. 2008. Differential projections from subfields in the lateral preoptic area to the lateral habenular complex of the rat. J Comp Neurol 507:1465-1478.
71. Lammel S, Ion DI, Roeper J, Malenka RC. 2011. Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron 70:855-862.
72. Lammel S, Lim BK, Ran C, Huang KW, Betley MJ, Tye KM, Deisseroth K, Malenka RC. 2012. Input-specific control of reward and aversion in the ventral tegmental area. Nature 491:212-217.
73. Lammel S, Lim BK, Malenka RC. 2014. Reward and aversion in a heterogeneous midbrain dopamine system. Neuropharmacology 76(Pt B):351-359.
74. Lavezzi HN, Zahm DS. 2011. The mesopontine rostromedial tegmental nucleus: an integrative modulator of the reward system. Basal Ganglia 1:191-200.
75. Lavezzi HN, Zahm DS. 2012. Structure and function of some non-habenular afferent projections to the mesopontine rostromedial tegmental nucleus. Soc Neurosci Abstr 183.14.
76. Lavezzi HN, Parsley KP, Zahm DS. 2012. Mesopontine rostromedial tegmental nucleus neurons projecting to the dorsal raphe and pedunculopontine tegmental nucleus: psychostimulant-elicited Fos expression and collateralization. Brain Struct Funct 217:719-734.
77. Lavezzi HN, Parsley KP, Zahm DS. 2014. Modulation of locomotor activation by the rostromedial tegmental nucleus. Neuropsychopharmacology 40:676-687.
78. Lecca S, Melis M, Luchicchi A, Ennas MG, Castelli MP, Muntoni AL, Pistis M. 2010. Effects of drugs of abuse on putative rostromedial tegmental neurons, inhibitory afferents to midbrain dopamine cells. Neuropsychopharmacology 36:589-602.
79. Lecca S, Melis M, Luchicchi A, Muntoni AL, Pistis M. 2011. Inhibitory inputs from rostromedial tegmental neurons regulate spontaneous activity of midbrain dopamine cells and their responses to drugs of abuse. Neuropsychopharmacology 37:1164-1176.
80. Lecourtier L, Kelly PH. 2007. A conductor hidden in the orchestra? Role of the habenular complex in monoamine transmission and cognition. Neurosci Biobehav Rev 31:658-672.
81. Lindvall O, Björkland A. 1983. Dopamine- and norepinephrine-containing neuron systems: their anatomy in the rat brain. In: Emson, PC, editor. Chemical neuroanatomy. New York: Raven Press. p 229-256.
82. Lodge DJ, Grace AA. 2006a. The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons. Proc Natl Acad Sci U S A 103:5167-5172.
83. Lodge DJ, Grace AA. 2006b. The hippocampus modulates dopamine neuron responsivity by regulating the intensity of phasic neuron activation. Neuropsychopharmacology 31:1356-1361.
84. Luskin MB, Price JL. 1983. The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J Comp Neurol 216:264-291.
85. Marinelli M, McCutcheon JE. 2014. Heterogeneity of dopamine neuron activity across traits and states. Neuroscience 282C:176-197.
86. Marinelli M, Rudick CN, Hu XT, White FJ. 2006. Excitability of dopamine neurons: modulation and physiological consequences. CNS Neurol Disord Drug Targets 5:79-97.
87. Matsui A, Williams JT. 2011. Opioid-sensitive GABA inputs from rostromedial tegmental nucleus synapse onto midbrain dopamine neurons. J Neurosci 31:17729-17735.
88. Matsui A, Jarvie BC, Robinson BG, Hentges ST, Williams JT. 2014. Separate GABA afferents to dopamine neurons mediate acute action of opioids, development of tolerance, and expression of withdrawal. Neuron 82:1346-1356.
89. Matsumoto M, Hikosaka O. 2007. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447:1111-1115.
90. Matsumoto M, Hikosaka O. 2008. Representation of negative motivational value in the primate lateral habenula. Nat Neurosci 12:77-84.
91. Matsumoto M, Hikosaka O. 2009. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459:837-841.
92. Mogenson GJ, Nielsen MA. 1983. Evidence that an accumbens to subpallidal GABAergic projection contributes to locomotor activity. Brain Res Bull 11:309-314.
93. Mogenson GJ, Yang CR. 1991. The contribution of basal forebrain to limbic-motor integration and the mediation of motivation to action. In: Napier TC, Kaliavs PW, Hanin I, editors. The basal forebrain. Anatomy to function. New York: Plenum Press (Adv Exp Med Biol 295). p 267-290.
94. Mogenson GJ, Swanson LW, Wu M. 1983. Neural projections from nucleus accumbens to globus pallidus, substantia innominata, and lateral preoptic-lateral hypothalamic area: an anatomical and electrophysiological investigation in the rat. J Neurosci 3:189-202.
95. Mogenson GJ, Swanson LW, Wu M. 1985. Evidence that projections from substantia innominata to zona incerta and mesencephalic locomotor region contribute to locomotor activity. Brain Res 334:65-76.
96. Mogenson, GJ, Brudzynski SM, Wu M, Yang CR, Yim CY. 1993. From motivation to action: a review of dopaminergic regulation of limbic-nucleus accumbens-ventral pallidum-pedunculopontine nucleus circuitries involved in limbic-motor integration. In: Kalivas PW, Barnes CD, editors. Limbic motor circuits and neuropsychiatry. Boca Raton, FL: CRC Press (Adv Exp Med Biol 295). p. 193-236.
97. Morales MF, Wang H, Zhang P, Lehrmann E, Wook WH, Becker KG, Ikemotor S, Jhou TC. 2011. Expression of prepronociceptin mRNA in the rostromedial tegmental nucleus (RMTg). Soc Neurosci Abstr 201.20.
98. Newman DB, Ginsberg CY. 1992. Brainstem reticular nuclei that project to the cerebellum in rats: a retrograde tracer study. Brain Behav Evol 39:24-68.
99. Nieuwenhuys R, Geeraedts LM, Veening JG. 1982. The medial forebrain bundle of the rat. I. General introduction. J Comp Neurol 206:49-81.
100. Oades RD, Halliday GM. 1987. Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res 434:117-165.
101. Omelchenko N, Bell R, Sesack SR. 2009. Lateral habenula projections to dopamine and GABA neurons in the rat ventral tegmental area. Eur J Neurosci 30:1239-1250.
102. Paxinos G, Watson C. 2007. The rat brain in stereotaxic coordinates, 6th ed. San Diego: Academic Press.
103. Paxinos G, Carrive P, Wang H, Wang PY. 1999. Chemoarchitectonic atlas of the rat brainstem. San Diego: Academic Press.
104. Perrotti LI, Bolanos CA, Cho, KH, Russo SJ, Edwards S, Ulery PG, Wallace DL, Self DW, Nestler EJ, Barrot M. 2005. DeltaFosB accumulates in a GABAergic cell population in the posterior tail of the ventral tegmental area after psychostimulant treatment. Eur J Neurosci 21:2817-2824.
105. Phillipson OT. 1979. Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: a horseradish peroxidase study in the rat. J Comp Neurol 187:117-143.
106. Pisotta I, Molinari M. 2014. Cerebellar contribution to feedforward control of locomotion. Front Hum Neurosci 8:475.
107. Rebec GV, Grabner CP, Johnson M, Pierce RC, Bardo MT. 1997a. Transient increases in catecholaminergic activity in medial prefrontal cortex and nucleus accumbens shell during novelty. Neuroscience 76:707-714.
108. Rebec GV, Christensen JCR, Guerra C, Bardo MT. 1997b. Regional and temporal differences in real-time dopamine efflux in the nucleus accumbens during free-choice novelty. Brain Res 776:61-67.
109. Reynolds SM, Zahm DS. 2005. Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala. J Neurosci 25:11757-11767.
110. Roby D, Yetnikoff L, Parsley KP, Zahm DS. 2014. A novel afferent of the ventral tegmental area and substantia nigra compacta from the deep frontal lobe. Soc Neurosci Abstr 442.05.
111. Saddoris MP, Sugam JA, Stuber GD, Witten IB, Deisseroth K, Carelli RM. 2014. Mesolimbic dopamine dynamically tracks, and is causally linked to, discrete aspects of value-based decision making. Biol Psychiatry 77:903-911.
112. Sahibzada N, Dean P, Redgrave P. 1986. Movements resembling orientation or avoidance elicited by electrical stimulation of the superior colliculus in rats. J Neurosci 6:723-733.
113. Salamone JD, Correa M. 2012. The mysterious motivational functions of mesolimbic dopamine. Neuron 76:470-485.
114. Scammell TE, Estabrooke IV, McCarthy MT, Chemelli RM, Yanagisawa M, Miller MS, Saper CB. 2000. Hypothalamic arousal regions are activated during modafinil-induced wakefulness. J Neurosci 20:8620-8628.
115. Schultz W. 1998. Predictive reward signal of dopamine neurons. J Neurophysiol 80:1-27.
116. Schultz W. 2007. Behavioral dopamine signals. Trends Neurosci 30:203-210.
117. Schultz W. 2013. Updating dopamine reward signals. Curr Opin Neurobiol 23:229-238.
118. Schultz W, Dayan P, Montague PR. 1997. A neural substrate of prediction and reward. Science 275:1593-1599.
119. Schulz S, Schreff M, Koch T, Zimprich A, Gramsch C, Elde R, Höllt V . 1998. Immunolocalization of two mu-opioid receptor isoforms (MOR1 and MOR1B) in the rat central nervous system. Neuroscience 82:613-622.
120. Sego C, Goncalves L, Lima L, Furigo IC, Donato J Jr, Metzger M. 2014. Lateral habenula and the rostromedial tegmental nucleus innervate neurochemically distinct subdivisions of the dorsal raphe nucleus in the rat. J Comp Neurol 522:1454-1484.
121. Sesack SR, Grace AA. 2010. Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35:27-47.
122. Shabel SJ, Proulx CD, Trias A, Murphy RT, Malinow R. 2012. Input to the lateral habenula from the basal ganglia is excitatory, aversive, and suppressed by serotonin. Neuron 74:475-481.
123. Shelton L, Becerra L, Borsook D. 2012. Unmasking the mysteries of the habenula in pain and analgesia. Prog Neurobiol 96:208-219.
124. Shreve PE, Uretsky NJ. 1988. Effect of GABAergic transmission in the subpallidal region on the hypermotility response to the administration of excitatory amino acids and picrotoxin into the nucleus accumbens. Neuropharmacology 27:1271-1277.
125. Shreve PE, Uretsky NJ. 1989. AMPA, kainic acid, and N-methyl-D-aspartic acid stimulate locomotor activity after injection into the substantia innominata/lateral preoptic area. Pharmacol Biochem Behav 34:101-106.
126. Shreve PE, Uretsky NJ. 1991. GABA and glutamate interact in the substantia innominata/lateral preoptic area to modulate locomotor activity. Pharmacol Biochem Behav 38:385-388.
127. Stamatakis AM, Stuber GD. 2012. Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance. Nat Neurosci 15:1105-1107.
128. Steinberg EE, Keiflin R, Boivin JR, Witten IB, Deisseroth K, Janak PH. 2013. A causal link between prediction errors, dopamine neurons and learning. Nat Neurosci 16:966-973.
129. Stern CA, Do Monte FH, Gazarini L, Carobrez AP, Bertoglio LJ. 2010. Activity in prelimbic cortex is required for adjusting the anxiety response level during the elevated plus-maze retest. Neuroscience 170:214-222.
130. Stopper CM, Floresco SB. 2013. What's better for me? Fundamental role for lateral habenula in promoting subjective decision biases. Nat Neurosci 17:33-35.
131. Sutherland RJ. 1982. The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci Biobehav Rev 6:1-13.
132. Thach WT. 2014. Does the cerebellum initiate movement? Cerebellum 13:139-150.
133. Ungless MA. 2004. Dopamine: the salient issue. Trends Neurosci 27:702-706.
134. Ungless MA, Argilli E, Bonci A. 2010. Effects of stress and aversion on dopamine neurons: implications for addiction. Neurosci Biobehav Rev 35:151-156.
135. Velasquez KM, Molfese DL, Salas R. 2014. The role of the habenula in drug addiction. Front Hum Neurosci 8:174.
136. von Krosigk M, Smith AD. 1991. Descending projections from the substantia nigra and retrorubral field to the medullary and pontomedullary reticular formation. Eur J Neurosci 3:260-273.
137. von Krosigk M, Smith Y, Bolam JP, Smith AD. 1992. Synaptic organization of GABAergic inputs from the striatum and the globus pallidus onto neurons in the substantia nigra and retrorubral field which project to the medullary reticular formation. Neuroscience 50:531-549.
138. Wasserman DI, Wang HG, Rashid AJ, Josselyn SA, Yeomans JS. 2013. Cholinergic control of morphine-induced locomotion in rostromedial tegmental nucleus versus ventral tegmental area sites. Eur J Neurosci 38:2774-2785.
139. Wasserman DI, Tan JMJ, Kim J, Yeomans JS. 2014. Muscarinic control of rostromedial tegmental nucleus (RMTg) GABA neurons and morphine-induced locomotion. Soc Neurosci Abstr 364.02.
140. White FJ. 1996. Synaptic regulation of mesocorticolimbic dopamine neurons. Annu Rev Neurosci 19:405-436.
141. Willins DL, Wallace LJ, Miller DD, Uretsky NJ. 1992. alpha-Amino-3-hydroxy-5-methylisoxazole-4-propionate/kainate receptor antagonists in the nucleus accumbens and ventral pallidum decrease the hypermotility response to psychostimulant drugs. J Pharmacol Exp Ther 260:1145-1151.
142. Wise RA. 2004. Dopamine, learning and motivation. Nat Rev Neurosci 5:483-494.
143. Yetnikoff L, Chang AY, Schwartz ZM, Parsley KP, Zahm DS. 2013. Differences in numbers of neurons projecting to the ventral tegmental area and rostromedial tegmental nucleus from key structures in the reward/aversion network. Soc Neurosci Abstr 393.07.
144. Yetnikoff L, Lavezzi HN, Reichard RA, Zahm DS. 2014a. An update on the connections of the ventral mesencephalic dopaminergic complex. Neuroscience 282C:23-48.
145. Yetnikoff L, Reichard RA, Schwartz ZM, Parsely KP, Zahm DS. 2014b. Protracted maturation of forebrain afferent connections of the ventral tegmental area in the rat. J Comp Neurol 522:1031-1047.
146. Zahm DS. 2006. The evolving theory of basal forebrain functional-anatomical 'macrosystems.' Neurosci Biobehav Rev 30:148-172.
147. Zahm DS, Heimer L. 1993. Specificity in the efferent projections of the nucleus accumbens in the rat: comparison of the rostral pole projection patterns with those of the core and shell. J Comp Neurol 327:220-232.
148. Zahm DS, Jensen SL, Williams ES, Martin JR 3rd. 1999. Direct comparison of projections from the central amygdaloid region and nucleus accumbens shell. Eur J Neurosci 11:1119-1126.
149. Zahm DS, Grosu S, Williams EA, Qin S, Berod A. 2001. Neurons of origin of the neurotensinergic plexus enmeshing the ventral tegmental area in rat: retrograde labeling and in situ hybridization combined. Neuroscience 104:841-851.
150. Zahm DS, Arends JJA, Parsley KP, Geisler S. 2011a. Projection to the mesopontine rostromedial tegmental nucleus from the lateral preoptic area. Soc Neurosci Abstr 79.09.
151. Zahm DS, Cheng AY, Lee TJ, Ghobadi CW, Schwartz ZM, Geisler S, Parsely KP, Gruber C, Veh RW. 2011b. Inputs to the midbrain dopaminergic complex in the rat, with emphasis on extended amygdala-recipient sectors. J Comp Neurol 519:3159-3188.
152. Zahm DS, Parsley KP, Schwartz ZM, Cheng AY. 2013. On lateral septum-like characteristics of outputs from the accumbal hedonic "hotspot" of Pecina and Berridge with commentary on the transitional nature of basal forebrain "boundaries." J Comp Neurol 521:50-68.
153. Zahm DS, Schwartz ZM, Lavezzi HN, Yetnikoff L, Parsley KP. 2014. Comparison of the locomotor-activating effects of bicuculline infusions into the preoptic area and ventral pallidum. Brain Struct Funct 219:511-526.