Ongoing behavioral state information signaled in the lateral habenula guides choice flexibility in freely moving rats

Frontiers in Behavioral Neuroscience

Volumn 9, Issue NOVEMBER, 2015, Pages

  Baker, Phillip M ^a   Oh, Sujean E ^a   Kidder, Kevan S ^a   Mizumori, Sheri J Y ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cognitive flexibility; Dopamine; Lateral habenula; Learning and memory; Reversal learning; Serotonin; Spatial navigation

Indexed keywords

BACLOFEN; MUSCIMOL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BEHAVIORAL FLEXIBILITY; CHOICE FLEXIBILITY; COMPARATIVE STUDY; CONTROLLED STUDY; DECISION MAKING; DOPAMINERGIC SYSTEM; EFFERENT NERVE; EXPERIMENTAL DESIGN; FUNCTIONAL ANATOMY; HABENULA; HISTOLOGY; LATERAL HABENULA; LEARNING; LOCAL FIELD POTENTIAL; MALE; NERVOUS SYSTEM PARAMETERS; NEUROPHYSIOLOGY; NONHUMAN; PROBABILISTIC REVERSAL LEARNING; RAT; REWARD; SENSORY NERVE; SEROTONINERGIC SYSTEM; SIGNAL TRANSDUCTION; SPATIAL MEMORY; SPATIAL ORIENTATION; TASK PERFORMANCE; THETA RHYTHM;

EID: 84947777458     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2015.00295     Document Type: Article

References (181)

1. Abercrombie, E. D., Keefe, K. A., DiFrischia, D. S., and Zigmond, M. J. (1989). Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens and medial frontal cortex. J. Neurochem. 52, 1655-1658. doi: 10.1111/j.1471-4159.1989.tb09224.x
2. Aizawa, H., Kobayashi, M., Tanaka, S., Fukai, T., and Okamoto, H. (2012). Molecular characterization of the subnuclei in rat habenula. J. Comp. Neurol. 520, 4051-4066. doi: 10.1002/cne.23167
3. Aizawa, H., Yanagihara, S., Kobayashi, M., Niisato, K., Takekawa, T., Harukuni, R., et al. (2013). The synchronous activity of lateral habenular neurons is essential for regulating hippocampal theta oscillation. J. Neurosci. 33, 8909-8921. doi: 10.1523/JNEUROSCI.4369-12.2013
4. Amodeo, D. A., Jones, J. H., Sweeney, J. A., and Ragozzino, M. E. (2012). Differences in BTBR T+ tf/J and C57BL/6J mice on probabilistic reversal learning and stereotyped behaviors. Behav. Brain Res. 227, 64-72. doi: 10.1016/j.bbr.2011.10.032
5. Andrade, T. G., Zangrossi, H., Jr., and Graeff, F. G. (2013). The median raphe nucleus in anxiety revisited. J. Psychopharmacol. 27, 1107-1115. doi: 10.1177/0269881113499208
6. Andres, K. H., von Düring, M., and Veh, R. W. (1999). Subnuclear organization of the rat habenular complexes. J. Comp. Neurol. 407, 130-150. doi: 10.1002/(sici)1096-9861(19990428)407:1<130::aid-cne10>3.0.co;2-8
7. Aragona, B. J., Day, J. J., Roitman, M. F., Cleaveland, N. A., Wightman, R. M., and Carelli, R. M. (2009). Regional specificity in the real-time development of phasic dopamine transmission patterns during acquisition of a cue-cocaine association in rats. Eur. J. Neurosci. 30, 1889-1899. doi: 10.1111/j.1460-9568.2009.07027.x
8. Araki, M., McGeer, P. L., and 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. doi: 10.1016/0006-8993(88)91410-2
9. Araki, M., McGeer, P. L., and McGeer, E. G. (1984). Retrograde HRP tracing combined with a pharmacohistochemical method for GABA transaminase for the identification of presumptive GABAergic projections to the habenula. Brain Res. 304, 271-277. doi: 10.1016/0006-8993(84)90330-5
10. Bachevalier, J., Nemanic, S., and Alvarado, M. C. (2015). The influence of context on recognition memory in monkeys: effects of hippocampal, parahippocampal and perirhinal lesions. Behav. Brain Res. 285, 89-98. doi: 10.1016/j.bbr.2014.07.010
11. Baker, P. M., Thompson, J. L., Sweeney, J. A., and Ragozzino, M. E. (2011). Differential effects of 5-HT(2A) and 5-HT(2C) receptor blockade on strategy- switching. Behav. Brain Res. 219, 123-131. doi: 10.1016/j.bbr.2010.12.031
12. Balcita-Pedicino, J. J., Omelchenko, N., Bell, R., and Sesack, S. R. (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. doi: 10.1002/cne.22561
13. Bari, A., Theobald, D. E., Caprioli, D., Mar, A. C., Aidoo-Micah, A., Dalley, J. W., et al. (2010). Serotonin modulates sensitivity to reward and negative feedback in a probabilistic reversal learning task in rats. Neuropsychopharmacology 35, 1290-1301. doi: 10.1038/npp.2009.233
14. Barlow, R. L., Alsiö, J., Jupp, B., Rabinovich, R., Shrestha, S., Roberts, A. C., et al. (2015). Markers of serotonergic function in the orbitofrontal cortex and dorsal raphe nucleus predict individual variation in spatial-discrimination serial reversal learning. Neuropsychopharmacology 40, 1619-1630. doi: 10.1038/npp.2014.335
15. Barnéoud, P., Descombris, E., Aubin, N., and Abrous, D. N. (2000). Evaluation of simple and complex sensorimotor behaviours in rats with a partial lesion of the dopaminergic nigrostriatal system. Eur. J. Neurosci. 12, 322-336. doi: 10.1046/j.1460-9568.2000.00896.x
16. Beckstead, R. M., Domesick, V. B., and Nauta, W. J. (1979). Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 175, 191-217. doi: 10.1016/0006-8993(79)91001-1
17. Benhamou, L., and Cohen, D. (2014). Electrophysiological characterization of entopeduncular nucleus neurons in anesthetized and freely moving rats. Front. Syst. Neurosci. 8:7. doi: 10.3389/fnsys.2014.00007
18. Berman, K. F., Zec, R. F., and Weinberger, D. R. (1986). Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia. II. Role of neuroleptic treatment, attention and mental effort. Arch. Gen. Psychiatry 43, 126-135. doi: 10.1001/archpsyc.1986.01800020032005
19. Bobillier, P., Seguin, S., Degueurce, A., Lewis, B. D., and Pujol, J. F. (1979). The efferent connections of the nucleus raphe centralis superior in the rat as revealed by radioautography. Brain Res. 166, 1-8. doi: 10.1016/0006-8993(79)90644-9
20. Bokil, H., Andrews, P., Kulkarni, J. E., Mehta, S., and Mitra, P. P. (2010). Chronux: a platform for analyzing neural signals. J. Neurosci. Methods 192, 146-151. doi: 10.1016/j.jneumeth.2010.06.020
21. Boulougouris, V., Glennon, J. C., and Robbins, T. W. (2008). Dissociable effects of selective 5-HT2A and 5-HT2C receptor antagonists on serial spatial reversal learning in rats. Neuropsychopharmacology 33, 2007-2019. doi: 10.1038/sj.npp.1301584
22. Brigman, J. L., Mathur, P., Harvey-White, J., Izquierdo, A., Saksida, L. M., Bussey, T. J., et al. (2010). Pharmacological or genetic inactivation of the serotonin transporter improves reversal learning in mice. Cereb. Cortex 20, 1955-1963. doi: 10.1093/cercor/bhp266
23. Brinschwitz, K., Dittgen, A., Madai, V. I., Lommel, R., Geisler, S., and Veh, R. W. (2010). Glutamatergic axons from the lateral habenula mainly terminate on GABAergic neurons of the ventral midbrain. Neuroscience 168, 463-476. doi: 10.1016/j.neuroscience.2010.03.050
24. Bromberg-Martin, E. S., Hikosaka, O., and Nakamura, K. (2010). Coding of task reward value in the dorsal raphe nucleus. J. Neurosci. 30, 6262-6272. doi: 10.1523/JNEUROSCI.0015-10.2010
25. Brown, H. D., Amodeo, D. A., Sweeney, J. A., and Ragozzino, M. E. (2012). The selective serotonin reuptake inhibitor, escitalopram, enhances inhibition of prepotent responding and spatial reversal learning. J. Psychopharmacol. 26, 1443-1455. doi: 10.1177/0269881111430749
26. Brown, H. D., McCutcheon, J. E., Cone, J. J., Ragozzino, M. E., and Roitman, M. F. (2011). Primary food reward and reward-predictive stimuli evoke different patterns of phasic dopamine signaling throughout the striatum. Eur. J. Neurosci. 34, 1997-2006. doi: 10.1111/j.1460-9568.2011.07914.x
27. Bryden, D. W., Burton, A. C., Kashtelyan, V., Barnett, B. R., and Roesch, M. R. (2012). Response inhibition signals and miscoding of direction in dorsomedial striatum. Front. Integr. Neurosci. 6:69. doi: 10.3389/fnint.2012.00069
28. Chavez-Martinez, M. E., Reyes-Vázquez, C., and Brust-Carmona, H. (1987). Lever pressing and active avoidance conditioning after electrolytic lesions of the entopeduncular nucleus in cats. Brain Res. Bull. 18, 279-284. doi: 10.1016/0361-9230(87)90003-7
29. Christoph, G. R., Leonzio, R. J., and Wilcox, K. S. (1986). Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmental area of the rat. J. Neurosci. 6, 613-619
30. Churchwell, J. C., Morris, A. M., Heurtelou, N. M., and Kesner, R. P. (2009). Interactions between the prefrontal cortex and amygdala during delay discounting and reversal. Behav. Neurosci. 123, 1185-1196. doi: 10.1037/a0017734
31. Cole, S., Hobin, M. P., and Petrovich, G. D. (2015). Appetitive associative learning recruits a distinct network with cortical, striatal and hypothalamic regions. Neuroscience 286, 187-202. doi: 10.1016/j.neuroscience.2014.11.026
32. Corbett, D., and Wise, R. A. (1979). Intracranial self-stimulation in relation to the ascending noradrenergic fiber systems of the pontine tegmentum and caudal midbrain: a moveable electrode mapping study. Brain Res. 177, 423-436. doi: 10.1016/0006-8993(79)90461-x
33. Crofts, H. S., Dalley, J. W., Collins, P., Van Denderen, J. C., Everitt, B. J., Robbins, T. W., et al. (2001). Differential effects of 6-OHDA lesions of the frontal cortex and caudate nucleus on the ability to acquire an attentional set. Cereb. Cortex 11, 1015-1026. doi: 10.1093/cercor/11.11.1015
34. Dacey, D. M., and Grossman, S. P. (1977). Aphagia, adipsia and sensory-motor deficits produced by amygdala lesions: a function of extra-amygdaloid damage. Physiol. Behav. 19, 389-395. doi: 10.1016/0031-9384(77)90284-0
35. Dalley, J. W., Cardinal, R. N., and Robbins, T. W. (2004). Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci. Biobehav. Rev. 28, 771-784. doi: 10.1016/j.neubiorev.2004.09.006
36. Darvas, M., Henschen, C. W., and Palmiter, R. D. (2014). Contributions of signaling by dopamine neurons in dorsal striatum to cognitive behaviors corresponding to those observed in parkinson’s disease. Neurobiol. Dis. 65, 112-123. doi: 10.1016/j.nbd.2014.01.017
37. De Steno, D. A., and Schmauss, C. (2009). A role for dopamine D2 receptors in reversal learning. Neuroscience 162, 118-127. doi: 10.1016/j.neuroscience.2009.04.052
38. Delgado, M. R., and Dickerson, K. C. (2012). Reward-related learning via multiple memory systems. Biol. Psychiatry 72, 134-141. doi: 10.1016/j.biopsych.2012.01.023
39. Dias, R., and Aggleton, J. P. (2000). Effects of selective excitotoxic prefrontal lesions on acquisition of nonmatching- and matching-to-place in the T-maze in the rat: differential involvement of the prelimbic-infralimbic and anterior cingulate cortices in providing behavioural flexibility. Eur. J. Neurosci. 12, 4457-4466. doi: 10.1046/j.0953-816x.2000.01323.x
40. Dickerson, K. C., Li, J., and Delgado, M. R. (2011). Parallel contributions of distinct human memory systems during probabilistic learning. Neuroimage 55, 266-276. doi: 10.1016/j.neuroimage.2010.10.080
41. Dickstein, D. P., Finger, E. C., Brotman, M. A., Rich, B. A., Pine, D. S., Blair, J. R., et al. (2010). Impaired probabilistic reversal learning in youths with mood and anxiety disorders. Psychol. Med. 40, 1089-1100. doi: 10.1017/s0033291709991462
42. Doya, K. (2008). Modulators of decision making. Nat. Neurosci. 11, 410-416. doi: 10.1038/nn2077
43. Dreyer, J. K., Herrik, K. F., Berg, R. W., and Hounsgaard, J. D. (2010). Influence of phasic and tonic dopamine release on receptor activation. J. Neurosci. 30, 14273-14283. doi: 10.1523/JNEUROSCI.1894-10.2010
44. Evers, E. A., van der Veen, F. M., Fekkes, D., and Jolles, J. (2007). Serotonin and cognitive flexibility: neuroimaging studies into the effect of acute tryptophan depletion in healthy volunteers. Curr. Med. Chem. 14, 2989-2995. doi: 10.2174/092986707782794032
45. Fallon, J. H. (1981). Collateralization of monoamine neurons: mesotelencephalic dopamine projections to caudate, septum and frontal cortex. J. Neurosci. 1, 1361-1368
46. Floresco, S. B., and Magyar, O. (2006). Mesocortical dopamine modulation of executive functions: beyond working memory. Psychopharmacology (Berl) 188, 567-585. doi: 10.1007/s00213-006-0404-5
47. Frank, M. J. (2005). Dynamic dopamine modulation in the basal ganglia: a neurocomputational account of cognitive deficits in medicated and nonmedicated parkinsonism. J. Cogn. Neurosci. 17, 51-72. doi: 10.1162/0898929052880093
48. Fries, P. (2005). A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 9, 474-480. doi: 10.1016/j.tics.2005.08.011
49. Geisler, S., Andres, K. H., and Veh, R. W. (2003). Morphologic and cytochemical criteria for the identification and delineation of individual subnuclei within the lateral habenular complex of the rat. J. Comp. Neurol. 458, 78-97. doi: 10.1002/cne.10566
50. Ghods-Sharifi, S., St Onge, J. R., and Floresco, S. B. (2009). Fundamental contribution by the basolateral amygdala to different forms of decision making. J. Neurosci. 29, 5251-5259. doi: 10.1523/JNEUROSCI.0315-09.2009
51. Gill, K. M., and Mizumori, S. J. Y. (2006). Context-dependent modulation by D1 receptors: differential effects in hippocampus and striatum. Behav. Neurosci. 120.377-392. doi: 10.1037/0735-7044.120.2.377
52. Goncalves, L., Sego, C., and 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. doi: 10.1002/cne.22787
53. Goto, Y., and Grace, A. A. (2005). Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat. Neurosci. 8, 805-812. doi: 10.1038/nn1471
54. Goutagny, R., Loureiro, M., Jackson, J., Chaumont, J., Williams, S., Isope, P., et al. (2013). Interactions between the lateral habenula and the hippocampus: implication for spatial memory processes. Neuropsychopharmacology 38, 2418-2426. doi: 10.1038/npp.2013.142
55. Greatrex, R. M., and Phillipson, O. T. (1982). Demonstration of synaptic input from prefrontal cortex to the habenula i the rat. Brain Res. 238, 192-197. doi: 10.1016/0006-8993(82)90782-x
56. Groman, S. M., James, A. S., Seu, E., Crawford, M. A., Harpster, S. N., and Jentsch, J. D. (2013). Monoamine levels within the orbitofrontal cortex and putamen interact to predict reversal learning performance. Biol. Psychiatry 73, 756-762. doi: 10.1016/j.biopsych.2012.12.002
57. Harris, J. A., Hirokawa, K. E., Sorensen, S. A., Gu, H., Mills, M., Ng, L. L., et al. (2014). Anatomical characterization of Cre driver mice for neural circuit mapping and manipulation. Front. Neural Circuits 8:76. doi: 10.3389/fncir.2014.00076
58. Herkenham, M., and Nauta, W. J. (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. doi: 10.1007/978-1-4684-920-1_16
59. Hervieu, G. (2003). Melanin-concentrating hormone functions in the nervous system: food intake and stress. Expert Opin. Ther. Targets 7, 495-511. doi: 10.1517/eott.7.4.495.22496
60. Heyser, C. J., Fienberg, A. A., Greengard, P., and Gold, L. H. (2000). DARPP-32 knockout mice exhibit impaired reversal learning in a discriminated operant task. Brain Res. 867, 122-130. doi: 10.1016/s0006-8993(00)02272-1
61. Hikosaka, O. (2010). The habenula: from stress evasion to value-based decision- making. Nat. Rev. Neurosci. 11, 503-513. doi: 10.1038/nrn2866
62. Hills, T. T. (2006). Animal foraging and the evolution of goal-directed cognition. Cogn. Sci. 30, 3-41. doi: 10.1207/s15516709cog0000_50
63. Hong, S., and Hikosaka, O. (2008). The globus pallidus sends reward-related signals to the lateral habenula. Neuron 60, 720-729. doi: 10.1016/j.neuron.2008.09.035
64. Inaba, K., Mizuhiki, T., Setogawa, T., Toda, K., Richmond, B. J., and Shidara, M. (2013). Neurons in monkey dorsal raphe nucleus code beginning and progress of step-by-step schedule, reward expectation and amount of reward outcome in the reward schedule task. J. Neurosci. 33, 3477-3491. doi: 10.1523/JNEUROSCI.4388-12.2013
65. Izquierdo, A., Carlos, K., Ostrander, S., Rodriguez, D., McCall-Craddolph, A., Yagnik, G., et al. (2012). Impaired reward learning and intact motivation after serotonin depletion in rats. Behav. Brain Res. 233, 494-499. doi: 10.1016/j.bbr.2012.05.032
66. Jo, Y. S., Lee, J., and Mizumori, S. J. (2013). Effects of prefrontal cortical inactivation on neural activity in the ventral tegmental area. J. Neurosci. 33, 8159-8171. doi: 10.1523/JNEUROSCI.0118-13.2013
67. Johnston, K., Levin, H. M., Koval, M. J., and Everling, S. (2007). Top-down control-signal dynamics in anterior cingulate and prefrontal cortex neurons following task switching. Neuron 53, 453-462. doi: 10.1016/j.neuron.2006.12.023
68. Joshua, M., Adler, A., Rosin, B., Vaadia, E., and Bergman, H. (2009). Encoding of probabilistic rewarding and aversive events by pallidal and nigral neurons. J. Neurophysiol. 101, 758-772. doi: 10.1152/jn.90764.2008
69. Kehagia, A. A., Murray, G. K., and Robbins, T. W. (2010). Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation. Curr. Opin. Neurobiol. 20, 199-204. doi: 10.1016/j.conb.2010.01.007
70. Kim, S. M., and Frank, L. M. (2009). Hippocampal lesions impair rapid learning of a continuous spatial alternation task. PLoS One 4:e5494. doi: 10.1371/journal.pone.0005494
71. Kim, U., and Chang, S. Y. (2005). Dendritic morphology, local circuitry and intrinsic electrophysiology of neurons in the rat medial and lateral habenular nuclei of the epithalamus. J. Comp. Neurol. 483, 236-250. doi: 10.1002/cne.20410
72. Kim, U., and Lee, T. (2012). Topography of descending projections from anterior insular and medial prefrontal regions to the lateral habenula of the epithalamus in the rat. Eur. J. Neurosci. 35, 1253-1269. doi: 10.1111/j.1460-9568.2012.08030.x
73. Kim, Y., Wood, J., and Moghaddam, B. (2012). Coordinated activity of ventral tegmental neurons adapts to appetitive and aversive learning. PLoS One 7:e29766. doi: 10.1371/journal.pone.0029766
74. Klanker, M., Feenstra, M., and Denys, D. (2013). Dopaminergic control of cognitive flexibility in humans and animals. Front. Neurosci. 7:201. doi: 10.3389/fnins.2013.00201
75. Koerts, J., Leenders, K. L., and Brouwer, W. H. (2009). Cognitive dysfunction in non-demented parkinson’s disease patients: controlled and automatic behavior. Cortex 45:922. doi: 10.1016/j.cortex.2009.02.014
76. Kosaki, Y., and Watanabe, S. (2012). Dissociable roles of the medial prefrontal cortex, the anterior cingulate cortex and the hippocampus in behavioural flexibility revealed by serial reversal of three-choice discrimination in rats. Behav. Brain Res. 227, 81-90. doi: 10.1016/j.bbr.2011.10.039
77. Kosse, C., and Burdakov, D. (2014). A unifying computational framework for stability and flexibility of arousal. Front. Syst. Neurosci. 8:192. doi: 10.3389/fnsys.2014.00192
78. Lapiz-Bluhm, M. D., Soto-Piña, A. E., Hensler, J. G., and Morilak, D. A. (2009). Chronic intermittent cold stress and serotonin depletion induce deficits of reversal learning in an attentional set-shifting test in rats. Psychopharmacology (Berl) 202, 329-341. doi: 10.1007/s00213-008-1224-6
79. Larkin, J. D., Jenni, N. L., and Floresco, S. B. (2015). Modulation of risk/reward decision making by dopaminergic transmission within the basolateral amygdala. Psychopharmacology (Berl) doi: 10.1007/s00213-015-4094-8 [Epub ahead of print]
80. Lecca, S., Meye, F. J., and Mameli, M. (2014). The lateral habenula in addiction and depression: an anatomical, synaptic and behavioral overview. Eur. J. Neurosci. 39, 1170-1178. doi: 10.1111/ejn.12480
81. Lecourtier, L., Defrancesco, A., and Moghaddam, B. (2008). Differential tonic influence of lateral habenula on prefrontal cortex and nucleus accumbens dopamine release. Eur. J. Neurosci. 27, 1755-1762. doi: 10.1111/j.1460-9568.2008.06130.x
82. Lecourtier, L., and Kelly, P. H. (2007). A conductor hidden in the orchestra? Role of the habenular complex in monoamine transmission and cognition. Neurosci. Biobehav. Rev. 31, 658-672. doi: 10.1016/j.neubiorev.2007.01.004
83. Lee, B., Groman, S., London, E. D., and Jentsch, J. D. (2007). Dopamine D2/D3 receptors play a specific role in the reversal of a learned visual discrimination in monkeys. Neuropsychopharmacology 32, 2125-2134. doi: 10.1038/sj.npp.1301337
84. Linseman, M. A. (1974). Inhibitory unit activity of the ventral forebrain during both appetitive and aversive pavlovian conditioning. Brain Res. 80, 146-151. doi: 10.1016/0006-8993(74)90733-1
85. Liu, Z., Zhou, J., Li, Y., Hu, F., Lu, Y., Ma, M., et al. (2014). Dorsal raphe neurons signal reward through 5-HT and glutamate. Neuron 81, 1360-1374. doi: 10.1016/j.neuron.2014.02.010
86. López Hill, X., Pascovich, C., Urbanavicius, J., Torterolo, P., and Scorza, M. C. (2013). The median raphe nucleus participates in the depressive-like behavior induced by MCH: differences with the dorsal raphe nucleus. Peptides 50, 96-99. doi: 10.1016/j.peptides.2013.10.002
87. Luo, X. F., Zhang, B. L., Li, J. C., Yang, Y. Y., Sun, Y. F., and Zhao, H. (2015). Lateral habenula as a link between dopaminergic and serotonergic systems contributes to depressive symptoms in parkinson’s disease. Brain Res. Bull. 110, 40-46. doi: 10.1016/j.brainresbull.2014.11.006
88. Lutjens, G., Krauss, J. K., and Schwabe, K. (2011). Lesions of the entopeduncular nucleus in rats prevent apomorphine-induced deficient sensorimotor gating. Behav. Brain Res. 220, 281-287. doi: 10.1016/j.bbr.2011.02.006
89. Margules, D. L. (1971). Localization of anti-punishment actions of norepinephrine and atropine in amygdala and entopeduncular nucleus of rats. Brain Res. 35, 177-184. doi: 10.1016/0006-8993(71)90603-2
90. Masaki, D., Yokoyama, C., Kinoshita, S., Tsuchida, H., Nakatomi, Y., Yoshimoto, K., et al. (2006). Relationship between limbic and cortical 5-HT neurotransmission and acquisition and reversal learning in a go/no-go task in rats. Psychopharmacology (Berl) 189, 249-258. doi: 10.1007/s00213-006-0559-0
91. Mathis, V., Cosquer, B., Avallone, M., Cassel, J. C., and Lecourtier, L. (2015). Excitatory transmission to the lateral habenula is critical for encoding and retrieval of spatial memory. Neuropsychopharmacology 40, 2843-2851. doi: 10.1038/npp.2015.140
92. Matsumoto, M., and Hikosaka, O. (2007). Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447, 1111-1115. doi: 10.1038/nature05860
93. Matsumoto, M., and Hikosaka, O. (2009). Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459, 837-841. doi: 10.1038/nature08028
94. McDevitt, R. A., Tiran-Cappello, A., Shen, H., Balderas, I., Britt, J. P., Marino, R. A., et al. (2014). Serotonergic versus nonserotonergic dorsal raphe projection neurons: differential participation in reward circuitry. Cell Rep. 8, 1857-1869. doi: 10.1016/j.celrep.2014.08.037
95. Means, L. W., and Holsten, R. D. (1992). Individual aged rats are impaired on repeated reversal due to loss of different behavioral patterns. Physiol. Behav. 52, 959-963. doi: 10.1016/0031-9384(92)90377-e
96. Mitra, P., and Bokil, H. (2007). Observed Brain Dynamics. New York, NY: Oxford University Press
97. Mizumori, S. J., Yeshenko, O., Gill, K. M., and Davis, D. M. (2004). Parallel processing across neural systems: implications for a multiple memory system hypothesis. Neurobiol. Learn. Mem. 82, 278-298. doi: 10.1016/j.nlm.2004.07.007
98. Mohler, E. G., Baker, P. M., Gannon, K. S., Jones, S. S., Shacham, S., Sweeney, J. A., et al. (2011). The effects of PRX-07034, a novel 5-HT(6) antagonist, on cognitive flexibility and working memory in rats. Psychopharmacology (Berl) 220, 687-696. doi: 10.1007/s00213-011-2518-7
99. Morice, R. (1990). Cognitive inflexibility and pre-frontal dysfunction in schizophrenia and mania. Br. J. Psychiatry 157, 50-54. doi: 10.1192/bjp.157.1.50
100. Nagy, J. I., Carter, D. A., Lehmann, J., and Fibiger, H. C. (1978). Evidence for a GABA-containing projection from the entopeduncular nucleus to the lateral habenula in the rat. Brain Res. 145, 360-364. doi: 10.1016/0006-8993(78)90869-7
101. Nakamura, K., Matsumoto, M., and Hikosaka, O. (2008). Reward-dependent modulation of neuronal activity in the primate dorsal raphe nucleus. J. Neurosci. 28, 5331-5343. doi: 10.1523/JNEUROSCI.0021-08.2008
102. Nesic, J., Rusted, J., Duka, T., and Jackson, A. (2011). Degree of dependence influences the effect of smoking on cognitive flexibility. Pharmacol. Biochem. Behav. 98, 376-384. doi: 10.1016/j.pbb.2011.01.015
103. Nikiforuk, A., and Popik, P. (2013). Amisulpride promotes cognitive flexibility in rats: the role of 5-HT7 receptors. Behav. Brain Res. 248, 136-140. doi: 10.1016/j.bbr.2013.04.008
104. Nikiforuk, A. (2012). Selective blockade of 5-HT7 receptors facilitates attentional set-shifting in stressed and control rats. Behav. Brain Res. 226, 118-123. doi: 10.1016/j.bbr.2011.09.006
105. Oades, R. D., and Halliday, G. M. (1987). Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res. 434, 117-165. doi: 10.1016/0165-0173(87)90011-7
106. O’Neill, M., and Brown, V. J. (2007). The effect of striatal dopamine depletion and the adenosine A2A antagonist KW-6002 on reversal learning in rats. Neurobiol. Learn. Mem. 88, 75-81. doi: 10.1016/j.nlm.2007.03.003
107. Ono, T., Nakamura, K., Nishijo, H., and Fukuda, M. (1986). Hypothalamic neuron involvement in integration of reward, aversion and cue signals. J. Neurophysiol. 56, 63-79
108. Ono, T., and Nakamura, K. (1985). Learning and integration of rewarding and aversive stimuli in the rat lateral hypothalamus. Brain Res. 346, 368-373. doi: 10.1016/0006-8993(85)90872-8
109. Panzeri, S., Schultz, S. R., Treves, A., and Rolls, E. T. (1999). Correlations and the encoding of information in the nervous system. Proc. Biol. Sci. 266, 1001-1012. doi: 10.1098/rspb.1999.0736
110. Parent, A., Gravel, S., and Boucher, R. (1981). The origin of forebrain afferents to the habenula in rat, cat and monkey. Brain Res. Bull. 6, 23-38. doi: 10.1016/s0361-9230(81)80066-4
111. Pennanen, L., van der Hart, M., Yu, L., and Tecott, L. H. (2013). Impact of serotonin (5-HT)2C receptors on executive control processes. Neuropsychopharmacology 38, 957-967. doi: 10.1038/npp.2012.258
112. Peyron, C., Tighe, D. K., van den Pol, A. N., de Lecea, L., Heller, H. C., Sutcliffe, J. G., et al. (1998). Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci. 18, 9996-10015
113. Phillips, A. G., Ahn, S., and Floresco, S. B. (2004). Magnitude of dopamine release in medial prefrontal cortex predicts accuracy of memory on a delayed response task. J. Neurosci. 24, 547-553. doi: 10.1523/jneurosci.4653-03.2004
114. Proulx, C. D., Hikosaka, O., and Malinow, R. (2014). Reward processing by the lateral habenula in normal and depressive behaviors. Nat. Neurosci. 17, 1146-1152. doi: 10.1038/nn.3779
115. Puryear, C. B., Kim, M. J., and Mizumori, S. J. (2010). Conjunctive encoding of movement and reward by ventral tegmental area neurons in the freely navigating rodent. Behav. Neurosci. 124, 234-247. doi: 10.1037/a0018865
116. Quina, L. A., Tempest, L., Ng, L., Harris, J. A., Ferguson, S., Jhou, T. C., et al. (2015). Efferent pathways of the mouse lateral habenula. J. Comp. Neurol. 523, 32-60. doi: 10.1002/cne.23662
117. Ragozzino, M. E. (2007). The contribution of the medial prefrontal cortex, orbitofrontal cortex and dorsomedial striatum to behavioral flexibility. Ann. N. Y. Acad. Sci. 1121, 355-375. doi: 10.1196/annals.1401.013
118. Ragozzino, M. E., Kim, J., Hassert, D., Minniti, N., and Kiang, C. (2003). The contribution of the rat prelimbic-infralimbic areas to different forms of task switching. Behav. Neurosci. 117, 1054-1065. doi: 10.1037/0735-7044.117.5.1054
119. Ragozzino, M. E., and Rozman, S. (2007). The effect of rat anterior cingulate inactivation on cognitive flexibility. Behav. Neurosci. 121, 698-706. doi: 10.1037/0735-7044.121.4.698
120. Ragozzino, M. E. (2002). The effects of dopamine D(1) receptor blockade in the prelimbic-infralimbic areas on behavioral flexibility. Learn. Mem. 9, 18-28. doi: 10.1101/lm.45802
121. Redila, V., Kinzel, C., Jo, Y. S., Puryear, C. B., and Mizumori, S. J. (2015). A role for the lateral dorsal tegmentum in memory and decision neural circuitry. Neurobiol. Learn. Mem. 117, 93-108. doi: 10.1016/j.nlm.2014.05.009
122. Ridley, R. M., Cummings, R. M., Leow-Dyke, A., and Baker, H. F. (2006). Neglect of memory after dopaminergic lesions in monkeys. Behav. Brain Res. 166, 253-262. doi: 10.1016/j.bbr.2005.08.007
123. Robbins, T. W., and Arnsten, A. F. (2009). The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. Annu. Rev. Neurosci. 32, 267-287. doi: 10.1146/annurev.neuro.051508.135535
124. Roberge, A. G., Boisvert, C., and Everett, J. (1980). Monoamine roles in retention and reversal of delayed response in cats. Pharmacol. Biochem. Behav. 12, 229-234. doi: 10.1016/0091-3057(80)90361-5
125. Rompre, P. P., and Miliaressis, E. (1985). Pontine and mesencephalic substrates of self-stimulation. Brain Res. 359, 246-259. doi: 10.1016/0006-8993(85)91435-0
126. Saito, Y., and Nagasaki, H. (2008). The melanin-concentrating hormone system and its physiological functions. Results Probl. Cell Differ. 46, 159-179. doi: 10.1007/400_2007_052
127. Sarkisov, G. T., Karapetyan, L. M., and Sarkisyan Zh, S. (2003). The effects of lesioning of the entopeduncular nucleus on the behavior of rats in simultaneous discrimination and open field conditions. Neurosci. Behav. Physiol. 33, 349-351. doi: 10.1023/A:1022891422772
128. Sartorius, A., Kiening, K. L., Kirsch, P., von Gall, C. C., Haberkorn, U., Unterberg, A. W., et al. (2010). Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient. Biol. Psychiatry 67, e9-e11. doi: 10.1016/j.biopsych.2009.08.027
129. Savitz, J. B., Nugent, A. C., Bogers, W., Roiser, J. P., Bain, E. E., Neumeister, A., et al. (2011). Habenula volume in bipolar disorder and major depressive disorder: a high-resolution magnetic resonance imaging study. Biol. Psychiatry 69, 336-343. doi: 10.1016/j.biopsych.2010.09.027
130. Scheel-Krüger, J., Magelund, G., and Olianas, M. (1981). The role of GABA in the basal ganglia and limbic system for behaviour. Adv. Biochem. Psychopharmacol. 29, 23-36.
131. Schultz, W. (1998). Predictive reward signal of dopamine neurons. J. Neurophysiol. 80, 1-27
132. Schwabe, K., Polikashvili, N., and Krauss, J. K. (2009). Deficient sensorimotor gating induced by selective breeding in rats is improved by entopeduncular nucleus lesions. Neurobiol. Dis. 34, 351-356. doi: 10.1016/j.nbd.2009.02.004
133. Schwartzbaum, J. S., and Donovick, P. J. (1968). Discrimination reversal and spatial alternation associated with septal and caudate dysfunction in rats. J. Comp. Physiol. Psychol. 65, 83-92. doi: 10.1037/h0025394
134. Seamans, J. K., Floresco, S. B., and Phillips, A. G. (1995). Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. Behav. Neurosci. 109, 1063-1073. doi: 10.1037/0735-7044.109.6.1063
135. Seamans, J. K., and Phillips, A. G. (1994). Selective memory impairments produced by transient lidocaine-induced lesions of the nucleus accumbens in rats. Behav. Neurosci. 108, 456-468. doi: 10.1037/0735-7044.108.3.456
136. Sego, C., Gonçalves, L., Lima, L., Furigo, I. C., 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. doi: 10.1002/cne.23533
137. Shabel, S. J., Proulx, C. D., Piriz, J., and Malinow, R. (2014). Mood regulation. GABA/glutamate co-release controls habenula output and is modified by antidepressant treatment. Science 345, 1494-1498. doi: 10.1126/science.1250469
138. Sharp, P. E., Turner-Williams, S., and Tuttle, S. (2006). Movement-related correlates of single cell activity in the interpeduncular nucleus and habenula of the rat during a pellet-chasing task. Behav. Brain Res. 166, 55-70. doi: 10.1016/j.bbr.2005.07.004
139. Shaw, C. L., Watson, G. D., Hallock, H. L., Cline, K. M., and Griffin, A. L. (2013). The role of the medial prefrontal cortex in the acquisition, retention and reversal of a tactile visuospatial conditional discrimination task. Behav. Brain Res. 236, 94-101. doi: 10.1016/j.bbr.2012.08.024
140. Shen, X., Ruan, X., and Zhao, H. (2012). Stimulation of midbrain dopaminergic structures modifies firing rates of rat lateral habenula neurons. PLoS One 7:e34323. doi: 10.1371/journal.pone.0034323
141. Shepard, P. D., Holcomb, H. H., and Gold, J. M. (2006). Schizophrenia in translation: the presence of absence: habenular regulation of dopamine neurons and the encoding of negative outcomes. Schizophr. Bull. 32, 417-421. doi: 10.1093/schbul/sbj083
142. Shohamy, D., Myers, C. E., Hopkins, R. O., Sage, J., and Gluck, M. A. (2009). Distinct hippocampal and basal ganglia contributions to probabilistic learning and reversal. J. Cogn. Neurosci. 21, 1821-1833. doi: 10.1162/jocn.2009.21138
143. Sim, L. J., and Joseph, S. A. (1992). Efferent projections of the nucleus raphe magnus. Brain Res. Bull. 28, 679-682. doi: 10.1016/0361-9230(92)90246-t
144. Skagerberg, G., Lindvall, O., and Björklund, A. (1984). Origin, course and termination of the mesohabenular dopamine pathway in the rat. Brain Res 307, 99-108. doi: 10.1016/0006-8993(84)90465-7
145. Skofitsch, G., Jacobowitz, D. M., and Zamir, N. (1985). Immunohistochemical localization of a melanin concentrating hormone-like peptide in the rat brain. Brain Res. Bull. 15, 635-649. doi: 10.1016/0361-9230(85)90213-8
146. Smith, D. M., and Mizumori, S. J. (2006). Hippocampal place cells, context and episodic memory. Hippocampus 16, 716-729. doi: 10.1002/hipo.20208
147. Sohn, J. W., Elmquist, J. K., and Williams, K. W. (2013). Neuronal circuits that regulate feeding behavior and metabolism. Trends Neurosci. 36, 504-512. doi: 10.1016/j.tins.2013.05.003
148. Spirduso, W. W., Gilliam, P. E., Schallert, T., Upchurch, M., Vaughn, D. M., and Wilcox, R. E. (1985). Reactive capacity: a sensitive behavioral marker of movement initiation and nigrostriatal dopamine function. Brain Res. 335, 45-54. doi: 10.1016/0006-8993(85)90274-4
149. Stamatakis, A. M., and Stuber, G. D. (2012). Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance. Nat. Neurosci. 15, 1105-1107. doi: 10.1038/nn.3145
150. Stefani, M. R., and Moghaddam, B. (2006). Rule learning and reward contingency are associated with dissociable patterns of dopamine activation in the rat prefrontal cortex, nucleus accumbens and dorsal striatum. J. Neurosci. 26, 8810-8818. doi: 10.1523/jneurosci.1656-06.2006
151. Stopper, C. M., and Floresco, S. B. (2014). What’s better for me? Fundamental role for lateral habenula in promoting subjective decision biases. Nat. Neurosci. 17, 33-35. doi: 10.1038/nn.3587
152. Stopper, C. M., Tse, M. T., Montes, D. R., Wiedman, C. R., and Floresco, S. B. (2014). Overriding phasic dopamine signals redirects action selection during risk/reward decision making. Neuron 84, 177-189. doi: 10.1016/j.neuron.2014.08.033
153. Stratford, T. R., and Wirtshafter, D. (2012). Evidence that the nucleus accumbens shell, ventral pallidum and lateral hypothalamus are components of a lateralized feeding circuit. Behav. Brain Res. 226, 548-554. doi: 10.1016/j.bbr.2011.10.014
154. Stuber, G. D., Klanker, M., de Ridder, B., Bowers, M. S., Joosten, R. N., Feenstra, M. G., et al. (2008). Reward-predictive cues enhance excitatory synaptic strength onto midbrain dopamine neurons. Science 321, 1690-1692. doi: 10.1126/science.1160873
155. Sutherland, R. J. (1982). The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci. Biobehav. Rev. 6, 1-13. doi: 10.1016/0149-7634(82)90003-3
156. Swanson, L. W. (1982). The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 9, 321-353. doi: 10.1016/0361-9230(82)90145-9
157. Taghzouti, K., Louilot, A., Herman, J. P., Le Moal, M., and Simon, H. (1985). Alternation behavior, spatial discrimination and reversal disturbances following 6-hydroxydopamine lesions in the nucleus accumbens of the rat. Behav. Neural Biol. 44, 354-363. doi: 10.1016/s0163-1047(85)90640-5
158. Thornton, E. W., and Bradbury, G. E. (1989). Effort and stress influence the effect of lesion of the habenula complex in one-way active avoidance learning. Physiol. Behav. 45, 929-935. doi: 10.1016/0031-9384(89)90217-5
159. Thornton, E. W., and Davies, C. (1991). A water-maze discrimination learning deficit in the rat following lesion of the habenula. Physiol. Behav. 49, 819-822. doi: 10.1016/0031-9384(91)90324-h
160. Thornton, E. W., and Evans, J. A. (1984). The effects of lesions of the habenula nucleus on lever press behaviour during a tandem operant schedule with contrasting response requirements. Behav. Brain Res. 12, 327-334. doi: 10.1016/0166-4328(84)90158-x
161. Thornton, E. W., Murray, M., Connors-Eckenrode, T., and Haun, F. (1994). Dissociation of behavioral changes in rats resulting from lesions of the habenula versus fasciculus retroflexus and their possible anatomical substrates. Behav. Neurosci. 108, 1150-1162. doi: 10.1037/0735-7044.108.6.1150
162. van der Kooy, D., and Carter, D. A. (1981). The organization of the efferent projections and striatal afferents of the entopeduncular nucleus and adjacent areas in the rat. Brain Res. 211, 15-36. doi: 10.1016/0006-8993(81)90064-0
163. van der Meulen, J. A., Joosten, R. N., de Bruin, J. P., and Feenstra, M. G. (2007). Dopamine and noradrenaline efflux in the medial prefrontal cortex during serial reversals and extinction of instrumental goal-directed behavior. Cereb. Cortex 17, 1444-1453. doi: 10.1093/cercor/bhl057
164. van der Plasse, G., and Feenstra, M. G. (2008). Serial reversal learning and acute tryptophan depletion. Behav. Brain Res. 186, 23-31. doi: 10.1016/j.bbr.2007.07.017
165. van Holst, R. J., and Schilt, T. (2011). Drug-related decrease in neuropsychological functions of abstinent drug users. Curr. Drug Abuse Rev. 4, 42-56. doi: 10.2174/1874473711104010042
166. Vasudeva, R. K., Lin, R. C., Simpson, K. L., and Waterhouse, B. D. (2011). Functional organization of the dorsal raphe efferent system with special consideration of nitrergic cell groups. J. Chem. Neuroanat. 41, 281-293. doi: 10.1016/j.jchemneu.2011.05.008
167. Vertes, R. P., Fortin, W. J., and Crane, A. M. (1999). Projections of the median raphe nucleus in the rat. J. Comp. Neurol. 407, 555-582. doi: 10.1002/(sici)1096-9861(19990517)407:4<555::aid-cne7>3.0.co;2-e
168. Vincent, S. R., and Brown, J. C. (1986). Somatostatin immunoreactivity in the entopeduncular projection to the lateral habenula in the rat. Neurosci. Lett. 68, 160-164. doi: 10.1016/0304-3940(86)90134-5
169. Volman, S. F., Lammel, S., Margolis, E. B., Kim, Y., Richard, J. M., Roitman, M. F., et al. (2013). New insights into the specificity and plasticity of reward and aversion encoding in the mesolimbic system. J. Neurosci. 33, 17569-17576. doi: 10.1523/JNEUROSCI.3250-13.2013
170. Wagner, F., Stroh, T., and Veh, R. W. (2014). Correlating habenular subnuclei in rat and mouse by using topographic, morphological and cytochemical criteria. J. Comp. Neurol. 522, 2650-2662. doi: 10.1002/cne.23554
171. Wallace, A., Pehrson, A. L., Sánchez, C., and Morilak, D. A. (2014). Vortioxetine restores reversal learning impaired by 5-HT depletion or chronic intermittent cold stress in rats. Int. J. Neuropsychopharmacol 17, 1695-1706. doi: 10.1017/S1461145714000571
172. Walshaw, P. D., Alloy, L. B., and Sabb, F. W. (2010). Executive function in pediatric bipolar disorder and attention-deficit hyperactivity disorder: in search of distinct phenotypic profiles. Neuropsychol. Rev. 20, 103-120. doi: 10.1007/s11065-009-9126-x
173. Wassum, K. M., and Izquierdo, A. (2015). The basolateral amygdala in reward learning and addiction. Neurosci. Biobehav. Rev. doi: 10.1016/j.neubiorev.2015.08.017 [Epub ahead of print].
174. Wassum, K. M., Ostlund, S. B., and Maidment, N. T. (2012). Phasic mesolimbic dopamine signaling precedes and predicts performance of a self-initiated action sequence task. Biol. Psychiatry 71, 846-854. doi: 10.1016/j.biopsych.2011.12.019
175. Waterhouse, B. D., Mihailoff, G. A., Baack, J. C., and Woodward, D. J. (1986). Topographical distribution of dorsal and median raphe neurons projecting to motor, sensorimotor and visual cortical areas in the rat. J. Comp. Neurol. 249, 460-476, 478-481. doi: 10.1002/cne.902490403
176. Wilcox, K. S., Christoph, G. R., Double, B. A., and Leonzio, R. J. (1986). Kainate and electrolytic lesions of the lateral habenula: effect on avoidance responses. Physiol. Behav. 36, 413-417. doi: 10.1016/0031-9384(86)90307-0
177. Winstanley, C. A., Theobald, D. E., Cardinal, R. N., and Robbins, T. W. (2004). Contrasting roles of basolateral amygdala and orbitofrontal cortex in impulsive choice. J. Neurosci. 24, 4718-4722. doi: 10.1523/jneurosci.5606-03.2004
178. Wirtshafter, D., and Asin, K. E. (1986). Discrimination learning and reversal following electrolytic lesions of the median raphe nucleus. Physiol. Behav. 37, 213-219. doi: 10.1016/0031-9384(86)90223-4
179. Wirtshafter, D. (2001). The control of ingestive behavior by the median raphe nucleus. Appetite 36, 99-105. doi: 10.1006/appe.2000.0373
180. Zangrossi, H., Jr., and Graeff, F. G. (2014). Serotonin in anxiety and panic: contributions of the elevated T-maze. Neurosci. Biobehav. Rev. 46, 397-406. doi: 10.1016/j.neubiorev.2014.03.007
181. Zweifel, L. S., Parker, J. G., Lobb, C. J., Rainwater, A., Wall, V. Z., Fadok, J. P., et al. (2009). Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior. Proc. Natl. Acad. Sci. U S A 106, 7281-7288. doi: 10.1073/pnas.0813415106