Circuit modules linking internal states and social behaviour in flies and mice

Nature Reviews Neuroscience

Volumn 17, Issue 11, 2016, Pages 692-704

  Anderson, David J ^a  

^a California Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRESSION; BEHAVIOR CONTROL; BRAIN NERVE CELL; COURTSHIP; DROSOPHILA MELANOGASTER; HYPOTHALAMUS; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; INTERNEURON; MATING; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; ANIMAL; ANIMAL MODEL; DRIVE; HUMAN; MOTIVATION; MOUSE; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY; PSYCHOLOGY;

AGGRESSION; ANIMALS; DRIVE; DROSOPHILA MELANOGASTER; HUMANS; MICE; MODELS, ANIMAL; MOTIVATION; NERVE NET; NEURONS; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR;

EID: 84992110560     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn.2016.125     Document Type: Review

References (150)

1. Anderson, D. J., & Adolphs, R. A framework for studying emotions across species. Cell 157, 187-200 (2014
2. LeDoux, J. Rethinking the emotional brain. Neuron 73, 653-676 (2012
3. Darwin, C. The Expression of the Emotions in Man and Animals (Univ. of Chicago Press, 1872
4. Lindquist, K. A., Siegel, E. H., Quigley, K. S., & Barrett, L. F. The hundred-year emotion war: are emotions natural kinds or psychological constructions? Comment on Lench, Flores, and Bench (2011). Psychol. Bull. 139, 255-263 (2011
5. Dethier, V. G. The Hungry Fly: a Physiological Study of the Behavior Associated With Feeding (Harvard Univ. Press, 1976
6. Berridge, K. C. Motivation concepts in behavioral neuroscience. Physiol. Behav. 81, 179-209 (2004
7. Tinbergen, N. The Study of Instinct (Clarendon Press, 1951
8. Lorenz, K., & Leyhausen, P. Motivation of Human and Animal Behavior (Van Nostrand Reinhold Company, 1973
9. Miczek, K. A., et al. Neurobiology of escalated aggression and violence. J. Neurosci. 27, 11803-11806 (2007
10. Lorenz, K. On Aggression (Harcourt, 1966
11. Palmer, C. R., Barnett, M. N., Copado, S., Gardezy, F., & Kristan, W. B. Multiplexed modulation of behavioral choice. J. Exp. Biol. 217, 2963-2973 (2014
12. Palmer, C. R., & Kristan, W. B. Contextual modulation of behavioral choice. Curr. Opin. Neurobiol. 21, 520-526 (2011
13. Beach, F. A. Analysis of factors involved in the arousal, maintenance and manifestation of sexual excitement in male animals. Psychosom. Med. 4, 173-198 (1942
14. Devidze, N., Lee, A., Zhou, J., & Pfaff, D. CNS arousal mechanisms bearing on sex and other biologically regulated behaviors. Physiol. Behav. 88, 283-293 (2006
15. Wu, M. V., & Shah, N. M. Control of masculinization of the brain and behavior. Curr. Opin. Neurobiol. 21, 116-123 (2011
16. Simerly, R. B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci. 25, 507-536 (2002
17. Morris, J. A., Jordan, C. L., & Breedlove, S. M. Sexual differentiation of the vertebrate nervous system. Nat. Neurosci. 7, 1034-1039 (2004
18. Manoli, D. S., Fan, P., Fraser, E. J., & Shah, N. M. Neural control of sexually dimorphic behaviors. Curr. Opin. Neurobiol. 23, 330-338 (2013
19. Pfaff, D., Westberg, L., & Kow, L. M. Generalized arousal of mammalian central nervous system. J. Comp. Neurol. 493, 86-91 (2005
20. Marder, E. Neuromodulation of neuronal circuits: back to the future. Neuron 76, 1-11 (2012
21. Veening, J. G., et al. Do similar neural systems subserve aggressive and sexual behaviour in male rats? Insights from c Fos and pharmacological studies. Eur. J. Pharmacol. 526, 226-239 (2005
22. Koganezawa, M., Kimura, K., & Yamamoto, D. The neural circuitry that functions as a switch for courtship versus aggression in Drosophila males. Curr. Biol. 26, 1395-1403 (2016
23. Yang, C. F., & Shah, N. M. Representing sex in the brain, one module at a time. Neuron 82, 261-278 (2014
24. Tinbergen, N. The hierarchical organization of nervous mechanisms underlying instinctive behaviour. Symp. Soc. Exp. Biol. 4, 305-312 (1950
25. Newman, S. W. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann. NY Acad. Sci. 877, 242-257 (1999
26. Auer, T. O., & Benton, R. Sexual circuitry in Drosophila. Curr. Opin. Neurobiol. 38, 18-26 (2016
27. Hashikawa, K., Hashikawa, Y., Falkner, A., & Lin, D. The neural circuits of mating and fighting in male mice. Curr. Opin. Neurobiol. 38, 27-37 (2016
28. Bayless, D. W., & Shah, N. M. Genetic dissection of neural circuits underlying sexually dimorphic social behaviours. Phil. Trans. R. Soc. B 371, 20150109 (2016
29. Yamamoto, D., Sato, K., & Koganezawa, M. Neuroethology of male courtship in Drosophila: from the gene to behavior. J. Comp. Physiol. A 200, 251-264 (2014
30. Yamamoto, D., & Koganezawa, M. Genes and circuits of courtship behaviour in Drosophila males. Nat. Rev. Neurosci. 14, 681-692 (2013
31. Bargmann, C. I., & Marder, E. From the connectome to brain function. Nat. Methods 10, 483-490 (2013
32. Bargmann, C. I. Beyond the connectome: how neuromodulators shape neural circuits. Bioessays 34, 458-465 (2012
33. Kravitz, E., & Huber, R. Aggression in invertebrates. Curr. Opin. Neurobiol. 13, 736-743 (2003
34. Huber, R., Smith, K., Delago, A., Isaksson, K., & Kravitz, E. A. Serotonin and aggressive motivation in crustaceans: altering the decision to retreat. Proc. Natl Acad. Sci. USA 94, 5939-5942 (1997
35. Stevenson, P. A., Dyakonova, V., Rillich, J., & Schildberger, K. Octopamine and experience-dependent modulation of aggression in crickets. J. Neurosci. 25, 1431-1441 (2005
36. Rillich, J., Schildberger, K., & Stevenson, P. A. Octopamine and occupancy: an aminergic mechanism for intruder-resident aggression in crickets. Proc. Biol. Sci. 278, 1873-1880 (2011
37. Stevenson, P. A., Hofmann, H. A., Schoch, K., & Schildberger, K. The fight and flight responses of crickets depleted of biogenic amines. J. Neurobiol. 43, 107-120 (2000
38. Chen, S., Lee, A. Y., Bowens, N. M., Huber, R., & Kravitz, E. A. Fighting fruit flies: a model system for the study of aggression. Proc. Natl Acad. Sci. USA 99, 5664-5668 (2002
39. Hoffmann, A. A laboratory study of male territoriality in the sibling species Drosophila melanogaster and Drosophila simulans. Animal Behav. 35, 807-818 (1987
40. Hoyer, S. C., et al. Octopamine in male aggression of Drosophila. Curr. Biol. 18, 159-167 (2008
41. Baier, A., Wittek, B., & Brembs, B. Drosophila as a new model organism for the neurobiology of aggression? J. Exp. Biol. 205, 1233-1240 (2002
42. Dierick, H. A., & Greenspan, R. J. Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nat. Genet. 39, 678-682 (2007
43. Alekseyenko, O. V., et al. Single serotonergic neurons that modulate aggression in Drosophila. Curr. Biol. 24, 2700-2707 (2014
44. Alekseyenko, O. V., Chan, Y. B., Li, R., & Kravitz, E. A. Single dopaminergic neurons that modulate aggression in Drosophila. Proc. Natl Acad. Sci. USA, 110, 6151-6156 (2013
45. Certel, S. J., et al. Octopamine neuromodulatory effects on a social behavior decision-making network in Drosophila males. PLoS ONE 5, e13248 (2010
46. Zhou, C., & Rao, Y. A subset of octopaminergic neurons are important for Drosophila aggression. Nat. Neurosci. 11, 1059-1067 (2008
47. Andrews, J. C., et al. Octopamine neuromodulation regulates Gr32a linked aggression and courtship pathways in Drosophila males. PLoS Genet. 10, e1004356 (2014
48. Roeder, T. Tyramine and octopamine: ruling behavior and metabolism. Annu. Rev. Entomol. 50, 447-477 (2005
49. Asahina, K., et al. Tachykinin-expressing neurons control male-specific aggressive arousal in Drosophila. Cell 156, 221-235 (2014
50. Halasz, J., et al. Substance P neurotransmission and violent aggression: the role of tachykinin NK1 receptors in the hypothalamic attack area. Eur. J. Pharmacol. 611, 35-43 (2009
51. Shaikh, M. B., Steinberg, A., & Siegel, A. Evidence that substance P is utilized in medial amygdaloid facilitation of defensive rage behavior in the cat. Brain Res. 625, 283-294 (1993
52. De Felipe, C., et al. Altered Nociception, Analgesia and Aggression in Mice Lacking the Receptor for Substance P. Nature 392, 394-397 (1998
53. Coccaro, E. F., Lee, R., Owens, M. J., Kinkead, B., & Nemeroff, C. B. Cerebrospinal fluid substance P like immunoreactivity correlates with aggression in personality disordered subjects. Biol. Psychiatry 72, 238-243 (2012
54. Correa, S. M., et al. An estrogen-responsive module in the ventromedial hypothalamus selectively drives sex-specific activity in females. Cell Rep. 10, 62-74 (2015
55. Lee, H., et al. Scalable control of mounting and attack by Esr1+ neurons in the ventromedial hypothalamus. Nature 509, 627-632 (2014
56. Taghert, P. H., & Nitabach, M. N. Peptide neuromodulation in invertebrate model systems. Neuron 76, 82-97 (2012
57. Katz, P. S., & Lillvis, J. L. Reconciling the deep homology of neuromodulation with the evolution of behavior. Curr. Opin. Neurobiol. 29, 39-47 (2014
58. Dickson, B. J. Wired for sex: the neurobiology of Drosophila mating decisions. Science 322, 904-909 (2008
59. Manoli, D. S., et al. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436, 395-400 (2005
60. Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirian, L., & Dickson, B. J. Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795-807 (2005
61. Cachero, S., Ostrovsky, A. D., Yu, J. Y., Dickson, B. J., & Jefferis, G. S. X. E. Sexual dimorphism in the fly brain. Curr. Biol. 20, 1589-1601 (2010
62. Yu, J. Y., Kanai, M. I., Demir, E., Jefferis, G. S. X. E., & Dickson, B. J. Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr. Biol. 20, 1602-1614 (2010
63. von Philipsborn, A. C., et al. Neuronal control of Drosophila courtship song. Neuron 69, 509-522 (2011
64. Kohatsu, S., & Yamamoto, D. Visually induced initiation of Drosophila innate courtship-like following pursuit is mediated by central excitatory state. Nat. Commun. 6, 6457 (2015
65. Kallman, B. R., Kim, H., & Scott, K. Excitation and inhibition onto central courtship neurons biases Drosophila mate choice. eLife 4, e11188 (2015
66. Clowney, E. J., Iguchi, S., Bussell, J. J., Scheer, E., & Ruta, V. Multimodal chemosensory circuits controlling male courtship in Drosophila. Neuron 87, 1036-1049 (2015
67. Hoopfer, E. D. Neural control of aggression in Drosophila. Curr. Opin. Neurobiol. 38, 109-118 (2016
68. Kohatsu, S., Koganezawa, M., & Yamamoto, D. Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 69, 498-508 (2011
69. Pan, Y., Meissner, G. W., & Baker, B. S. Joint control of Drosophila male courtship behavior by motion cues and activation of male-specific P1 neurons. Proc. Natl Acad. Sci. USA 109, 10065-10070 (2012
70. Kimura, K. I., Hachiya, T., Koganezawa, M., Tazawa, T., & Yamamoto, D. Fruitless and doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 59, 759-769 (2008
71. Zhou, C., Pan, Y., Robinett, C. C., Meissner, G. W., & Baker, B. S. Central brain neurons expressing doublesex regulate female receptivity in Drosophila. Neuron 83, 149-163 (2014
72. Rideout, E. J., Billeter, J. C., & Goodwin, S. F. The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr. BIol. 17, 1473-1478 (2007
73. Costa, M., Manton, J. D., Ostrovsky, A. D., Prohaska, S., & Jefferis, G. S. NBLAST: rapid, sensitive comparison of neuronal structure and construction of neuron family databases. Neuron 91, 293-311 (2016
74. Hoopfer, E. D., Jung, Y., Inagaki, H. K., Rubin, G. M., & Anderson, D. J. P1 interneurons promote a persistent internal state that enhances inter-male aggression in Drosophila. eLife 4, e11346 (2016
75. Inagaki, H. K., et al. Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship. Nat. Methods 11, 325-332 (2014
76. Jenett, A., et al. A GAL4 driver line resource for Drosophila neurobiology. Cell Rep. 2, 991-1001 (2012
77. Hamada, F. N., et al. An internal thermal sensor controlling temperature preference in Drosophila. Nature 454, 217-220 (2008
78. Luan, H., Peabody, N. C., Vinson, C. R., & White, B. H. Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 52, 425-436 (2006
79. Pfeiffer, B. D., et al. Refinement of tools for targeted gene expression in Drosophila. Genetics 186, 735-755 (2010
80. Lin, J. Y., Knutsen, P. M., Muller, A., Kleinfeld, D., & Tsien, R. Y. ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation. Nat. Neurosci. 16, 1499-1508 (2013
81. Klapoetke, N. C., et al. Independent optical excitation of distinct neural populations. Nat. Methods 11, 338-346 (2014
82. Bath, D. E., et al. FlyMAD: rapid thermogenetic control of neuronal activity in freely walking Drosophila. Nat. Methods 11, 756-762 (2014
83. Wang, L., Dankert, H., Perona, P., & Anderson, D. J. A common genetic target for environmental and heritable influences on aggressiveness in Drosophila. Proc. Natl Acad. Sci. USA 105, 5657-5663 (2008
84. Zhang, S. X., Rogulja, D., & Crickmore, M. A. Dopaminergic circuitry underlying mating drive. Neuron 91, 168-181 (2016
85. Beach, F. A., & Jordan, L. Sexual exhaustion and recovery in the male rat. Q. J. Exp. Psychol. 8, 121-133 (1956
86. Hess, W. R., & Brügger, M. Das subkortikale Zentrum Der affecktiven Abwehr-reaktion. Helv. Physiol. Acta 1, 33-52 (in German) (1943
87. Siegel, A., Roeling, T. A., Gregg, T. R., & Kruk, M. R. Neuropharmacology of brain-stimulation-evoked aggression. Neurosci. Biobehav. Rev. 23, 359-389 (1999
88. Kruk, M. R. in Neuroscience of Aggression (eds Meyer-Lindenberg, A., & Miczek, K. A.) (Springer, 2014
89. Kruk, M. R., et al. Discriminant analysis of the localization of aggression-inducing electrode placements in the hypothalamus of male rats. Brain Res. 260, 61-79 (1983
90. Hrabovszky, E., et al. Neurochemical characterization of hypothalamic neurons involved in attack behavior: glutamatergic dominance and co expression of thyrotropin-releasing hormone in a subset of glutamatergic neurons. Neuroscience 133, 657-666 (2005
91. Jorgenson, L. A., et al. The BRAIN Initiative: developing technology to catalyse neuroscience discovery. Phil. Trans. R. Soc. B 370, 20140164 (2015
92. Nelson, R. J., & Trainor, B. C. Neural mechanisms of aggression. Nat. Rev. Neurosci. 8, 536-546 (2007
93. Kruk, M. R. Ethology and pharmacology of hypothalamic aggression in the rat. Neurosci. Biobehav. Rev. 15, 527-538 (1991
94. Kim, Y., et al. Mapping social behavior-induced brain activation at cellular resolution in the mouse. Cell Rep. 10, 292-305 (2015
95. Kennedy, A., et al. Internal states and behavioral decision-making: toward an integration of emotion and cognition. Cold Spring Harb. Symp. Quant. Biol. 79, 199-210 (2015
96. Anderson, D. J. Optogenetics, sex, and violence in the brain: implications for psychiatry. Biol. Psychiatry 71, 1081-1089 (2012
97. Falkner, A. L., & Lin, D. Recent advances in understanding the role of the hypothalamic circuit during aggression. Front. Syst. Neurosci. 8, 168 (2014
98. Lin, D., et al. Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221-226 (2011
99. Yang, C. F., et al. Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell 153, 896-909 (2013
100. Sano, K., Tsuda, M. C., Musatov, S., Sakamoto, T., & Ogawa, S. Differential effects of site-specific knockdown of estrogen receptor α in the medial amygdala, medial pre-optic area, and ventromedial nucleus of the hypothalamus on sexual and aggressive behavior of male mice. Eur. J. Neurosci. 37, 1308-1319 (2013
101. Kunwar, P. S., et al. Ventromedial hypothalamic neurons control a defensive emotion state. eLife 4, e06633 (2015
102. Wang, L., Chen, I. Z., & Lin, D. Collateral pathways from the ventromedial hypothalamus mediate defensive behaviors. Neuron 85, 1-15 (2015
103. Hong, W., Kim, D. W., & Anderson, D. J. Antagonistic control of social versus repetitive self-grooming behaviors by separable amygdala neuronal subsets. Cell 158, 1348-1361 (2014
104. Swanson, L. W. Anatomy of the soul as reflected in the cerebral hemispheres: neural circuits underlying voluntary control of basic motivated behaviors. J. Comp. Neurol. 493, 122-131 (2005
105. Dong, H.-W., Petrovich, G. D., & Swanson, L. W. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Brain Res. Rev. 38, 192-246 (2001
106. Canteras, N. S., Simerly, R. B., & Swanson, L. W. Organization of projections from the ventromedial nucleus of the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J. Comp. Neurol. 348, 41-79 (2011
107. Lee, G., & Gammie, S. C. GABAA receptor signaling in caudal periaqueductal gray regulates maternal aggression and maternal care in mice. Behav. Brain Res. 213, 230-237 (2010
108. Pfaff, D. W., & Sakuma, Y. Facilitation of the lordosis reflex of female rats from the ventromedial nucleus of the hypothalamus. J. Physiol. 288, 189-202 (1979
109. Pfaff, D. W., & Sakuma, Y. Deficit in the lordosis reflex of female rats caused by lesions in the ventromedial nucleus of the hypothalamus. J. Physiol. 288, 203-210 (1979
110. Falkner, A. L., Dollar, P., Perona, P., Anderson, D. J., & Lin, D. Decoding ventromedial hypothalamic neural activity during male mouse aggression. J. Neurosci. 34, 5971-5984 (2014
111. Goldman, M., Compte, A., & Wang, X. J. in New Encyclopedia of Neuroscience (ed. Squire, L. R.) 1-26 (Elsevier, 2007
112. Ginsburg, B., & Allee, W. Some effects of conditioning on social dominance and subordination in inbred strains of mice. Physiol. Zool. 15, 485-506 (1942
113. Couppis, M. H., & Kennedy, C. H. The rewarding effect of aggression is reduced by nucleus accumbens dopamine receptor antagonism in mice. Psychopharmacology 197, 449-456 (2008
114. Falkner, A. L., Grosenick, L., Davidson, T. J., Deisseroth, K., & Lin, D. Hypothalamic control of male aggression-seeking behavior. Nat. Neurosci. 19, 596-604 (2016
115. Potegal, M., Hebert, M., DeCoster, M., & Meyerhoff, J. L. Brief, high-frequency stimulation of the corticomedial amygdala induces a delayed and prolonged increase of aggressiveness in male Syrian golden hamsters. Behav. Neurosci. 110, 401-412 (1996
116. Potegal, M. Time course of aggressive arousal in female hamsters and male rats. Behav. Neural Biol. 58, 120-124 (1992
117. Spiteri, T., et al. Estrogen-induced sexual incentive motivation, proceptivity and receptivity depend on a functional estrogen receptor α in the ventromedial nucleus of the hypothalamus but not in the amygdala. Neuroendocrinology 91, 142-154 (2010
118. De Velasco, B., et al. Specification and development of the pars intercerebralis and pars lateralis, neuroendocrine command centers in the Drosophila brain. Dev. Biol. 302, 309-323 (2007
119. Ziv, Y., et al. Long-term dynamics of CA1 hippocampal place codes. Nat. Neurosci. 16, 264-266 (2013
120. Jennings, J. H., et al. Visualizing hypothalamic network dynamics for appetitive and consummatory behaviors. Cell 160, 516-527 (2015
121. Tasic, B., et al. Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nat. Neurosci. 19, 335-346 (2016
122. Macosko, E. Z., et al. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 161, 1202-1214 (2015
123. von Holst, E., & von Saint Paul, U. On the functional organization of drives. J. Animal Behav. 11, 1-20 (1960
124. Grover, D., Katsuki, T., & Greenspan, R. J. Flyception: imaging brain activity in freely walking fruit flies. Nat. Methods 13, 569-572 (2016
125. Dong, H. W., & Swanson, L. W. Projections from bed nuclei of the stria terminalis, posterior division: implications for cerebral hemisphere regulation of defensive and reproductive behaviors. J. Comp. Neurol. 471, 396-433 (2004
126. Dulac, C., & Wagner, S. Genetic analysis of brain circuits underlying pheromone signaling. Annu. Rev. Genet. 40, 449-467 (2006
127. Toth, M., Fuzesi, T., Halász, J., Tulogdi, A., & Haller, J. Neural inputs of the hypothalamic aggression area in the rat. Behav. Brain Res. 215, 7-20 (2010
128. Root, C. M., Denny, C. A., Hen, R., & Axel, R. The participation of cortical amygdala in innate, odour-driven behaviour. Nature 515, 269-273 (2014
129. Mandiyan, V. S., Coats, J. K., & Shah, N. M. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nat. Neurosci. 8, 1660-1662 (2005
130. Yoon, H., Enquist, L. W., & Dulac, C. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 123, 669-682 (2005
131. Leypold, B. G., et al. Altered sexual and social behaviors in trp2 mutant mice. Proc. Natl Acad. Sci. USA 99, 6376-6381 (2002
132. Stowers, L., Holy, T. E., Meister, M., Dulac, C., & Koentges, G. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295, 1493-1500 (2002
133. Sachs, B. D. Erection evoked in male rats by airborne scent from estrous females. Physiol. Behav. 62, 921-924 (1997
134. Bensafi, M., Tsutsui, T., Khan, R., Levenson, R. W., & Sobel, N. Sniffing a human sex-steroid derived compound affects mood and autonomic arousal in a dose-dependent manner. Psychoneuroendocrinology 29, 1290-1299 (2004
135. Simerly, R. B., Chang, C., Muramatsu, M., & Swanson, L. W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J. Comp. Neurol. 294, 76-95 (1990
136. Shohat-Ophir, G., Kaun, K. R., Azanchi, R., & Heberlein, U. Sexual deprivation increases ethanol intake in Drosophila. Science 335, 1351-1355 (2012
137. Kristan, W. B. Neuronal decision-making circuits. Curr. Biol. 18, R928-R932 (2008
138. Kim, C. K., et al. Simultaneous fast measurement of circuit dynamics at multiple sites across the mammalian brain. Nat. Methods 13, 325-328 (2016
139. van Swinderen, B., & Andretic, R. Arousal in Drosophila. Behav. Processes 64, 133-144 (2003
140. Lebestky, T., et al. Two different forms of arousal in Drosophila are oppositely regulated by the dopamine D1 receptor ortholog DopR via distinct neural circuits. Neuron 64, 522-536 (2009
141. Sternson, S. M. Hypothalamic survival circuits: blueprints for purposive behaviors. Neuron 77, 810-824 (2013
142. Castro, D. C., & Berridge, K. C. Advances in the neurobiological bases for food ?liking? versus ?wanting?. Physiol. Behav. 136, 22-30 (2014
143. Berridge, K. C. Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns. Neurosci. Biobehav. Rev. 24, 173-198 (2000
144. Wustmann, G., Rein, K., Wolf, R., & Heisenberg, M. A new paradigm for operant conditioning of Drosophila melanogaster. J. Comp. Physiol. A 179, 429-436 (1996
145. Kaun, K. R., Azanchi, R., Maung, Z., Hirsh, J., & Heberlein, U. A Drosophila model for alcohol reward. Nat. Neurosci. 14, 612-619 (2011
146. Krashes, M. J., et al. A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139, 416-427 (2009
147. Dolan, R. J. Emotion, cognition, and behavior. Science 298, 1191-1194 (2002
148. Wu, M. V., et al. Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 139, 61-72 (2009
149. Kohl, J., Ostrovsky, A. D., Frechter, S., & Jefferis, G. S. X. E. A bidirectional circuit switch reroutes pheromone signals in male and female brains. Cell 155, 1610-1623 (2013
150. Ruta, V., et al. A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 468, 686-690 (2010