Medial amygdalar aromatase neurons regulate aggression in both sexes

Cell Reports

Volumn 10, Issue 4, 2015, Pages 453-462

  Unger, Elizabeth K ^a   Burke, Kenneth J ^a   Yang, Cindy F ^a   Bender, Kevin J ^b   Fuller, Patrick M ^c   Shah, Nirao M ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN FUNCTION; BRAIN REGION; CELL POPULATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME REGULATION; FEMALE; MALE; MEDIAL AMYGDALA; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SEX DIFFERENCE; SOCIAL INTERACTION; ANIMAL; ENZYMOLOGY; METABOLISM; NERVE CELL; PHYSIOLOGY; SEXUAL BEHAVIOR;

MUS; VERTEBRATA;

AGGRESSION; ANIMALS; AROMATASE; BEHAVIOR, ANIMAL; FEMALE; MALE; MICE; NEURONS; SEXUAL BEHAVIOR, ANIMAL;

EID: 84922832285     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.12.040     Document Type: Article

References (60)

1. Alexander G.M., Rogan S.C., Abbas A.I., Armbruster B.N., Pei Y., Allen J.A., Nonneman R.J., Hartmann J., Moy S.S., Nicolelis M.A., et al. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 2009, 63:27-39.
2. Anaclet C., Ferrari L., Arrigoni E., Bass C.E., Saper C.B., Lu J., Fuller P.M. The GABAergic parafacial zone is a medullary slow wave sleep-promoting center. Nat. Neurosci. 2014, 17:1217-1224.
3. Armbruster B.N., Li X., Pausch M.H., Herlitze S., Roth B.L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl. Acad. Sci. USA 2007, 104:5163-5168.
4. Arnold A.P. The organizational-activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Horm. Behav. 2009, 55:570-578.
5. Ball J. Sex activity of castrated male rats increased by estrin administration. J.Comp. Psychol. 1937, 24:135-144.
6. Balthazart J., Ball G.F. New insights into the regulation and function of brain estrogen synthase (aromatase). Trends Neurosci. 1998, 21:243-249.
7. Baum M.J., Bakker J. Roles of sex and gonadal steroids inmammalian pheromonal communication. Front. Neuroendocrinol. 2013, 34:268-284.
8. Bergan J.F., Ben-Shaul Y., Dulac C. Sex-specific processing of social cues in the medial amygdala. eLife 2014, 3:e02743.
9. Carney R.S.E., Mangin J.-M., Hayes L., Mansfield K., Sousa V.H., Fishell G., Machold R.P., Ahn S., Gallo V., Corbin J.G. Sonic hedgehog expressing and responding cells generate neuronal diversity in the medial amygdala. Neural Dev. 2010, 5:14.
10. Choi G.B., Dong H.-W., Murphy A.J., Valenzuela D.M., Yancopoulos G.D., Swanson L.W., Anderson D.J. Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 2005, 46:647-660.
11. De Vries G.J., Boyle P.A. Double duty for sex differences in the brain. Behav. Brain Res. 1998, 92:205-213.
12. Demas G.E., Kriegsfeld L.J., Blackshaw S., Huang P., Gammie S.C., Nelson R.J., Snyder S.H. Elimination of aggressive behavior in male mice lacking endothelial nitric oxide synthase. J.Neurosci. 1999, 19:RC30.
13. DiBenedictis B.T., Ingraham K.L., Baum M.J., Cherry J.A. Disruption of urinary odor preference and lordosis behavior in female mice given lesions of the medial amygdala. Physiol. Behav. 2012, 105:554-559.
14. Finney H.C., Erpino M.J. Synergistic effect of estradiol benzoate and dihydrotestosterone on aggression in mice. Horm. Behav. 1976, 7:391-400.
15. Forlano P.M., Schlinger B.A., Bass A.H. Brain aromatase: new lessons from non-mammalian model systems. Front. Neuroendocrinol. 2006, 27:247-274.
16. Gammie S.C., Nelson R.J. Maternal aggression is reduced in neuronal nitric oxide synthase-deficient mice. J.Neurosci. 1999, 19:8027-8035.
17. Gammie S.C., Huang P.L., Nelson R.J. Maternal aggression in endothelial nitric oxide synthase-deficient mice. Horm. Behav. 2000, 38:13-20.
18. Gandelman R. Mice: postpartum aggression elicited by the presence of an intruder. Horm. Behav. 1972, 3:23-28.
19. Hong W., Kim D.-W., Anderson D.J. Antagonistic control of social versus repetitive self-grooming behaviors by separable amygdala neuronal subsets. Cell 2014, 158:1348-1361.
20. Juntti S.A., Tollkuhn J., Wu M.V., Fraser E.J., Soderborg T., Tan S., Honda S., Harada N., Shah N.M. The androgen receptor governs the execution, but not programming, of male sexual and territorial behaviors. Neuron 2010, 66:260-272.
21. Keshavarzi S., Sullivan R.K.P., Ianno D.J., Sah P. Functional properties and projections of neurons in the medial amygdala. J.Neurosci. 2014, 34:8699-8715.
22. Kimura T., Hagiwara Y. Regulation of urine marking in male and female mice: effects of sex steroids. Horm. Behav. 1985, 19:64-70.
23. Lee H., Kim D.-W., Remedios R., Anthony T.E., Chang A., Madisen L., Zeng H., Anderson D.J. Scalable control of mounting and attack by Esr1+ neurons in the ventromedial hypothalamus. Nature 2014, 509:627-632.
24. MacLusky N.J., Naftolin F. Sexual differentiation of the central nervous system. Science 1981, 211:1294-1302.
25. Matsumoto T., Honda S., Harada N. Alteration in sex-specific behaviors in male mice lacking the aromatase gene. Neuroendocrinology 2003, 77:416-424.
26. McCarthy M.M. Estradiol and the developing brain. Physiol. Rev. 2008, 88:91-124.
27. McDermott N.J., Gandelman R. Exposure to young induces postpartum-like fighting in virgin female mice. Physiol. Behav. 1979, 23:445-448.
28. McGill T.E. Sexual behavior in three inbred strains of mice. Behavior 1962, 19:341-350.
29. Morgan C.W., Julien O., Unger E.K., Shah N.M., Wells J.A. Turning on caspases with genetics and small molecules. Methods Enzymol. 2014, 544:179-213.
30. Morris J.A., Jordan C.L., Breedlove S.M. Sexual differentiation of the vertebrate nervous system. Nat. Neurosci. 2004, 7:1034-1039.
31. Moyer K. Kinds of aggression and their physiological basis. Commun. Behav. Biol. 1968, 2:65-87.
32. Naftolin F., Ryan K.J., Petro Z. Aromatization of androstenedione by the diencephalon. J.Clin. Endocrinol. Metab. 1971, 33:368-370.
33. Nelson R.J., Demas G.E., Huang P.L., Fishman M.C., Dawson V.L., Dawson T.M., Snyder S.H. Behavioural abnormalities in male mice lacking neuronal nitric oxide synthase. Nature 1995, 378:383-386.
34. Nelson A.B., Hammack N., Yang C.F., Shah N.M., Seal R.P., Kreitzer A.C. Striatal cholinergic interneurons Drive GABA release from dopamine terminals. Neuron 2014, 82:63-70.
35. Nunez A.A., Nyby J., Whitney G. The effects of testosterone, estradiol, and dihydrotestosterone on male mouse (Mus musculus) ultrasonic vocalizations. Horm. Behav. 1978, 11:264-272.
36. Ogawa S., Chester A.E., Hewitt S.C., Walker V.R., Gustafsson J.A., Smithies O., Korach K.S., Pfaff D.W. Abolition of male sexual behaviors in mice lacking estrogen receptors alpha and beta (alpha beta ERKO). Proc. Natl. Acad. Sci. USA 2000, 97:14737-14741.
37. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates: Compact 2003, Academic Press, New York. Second Edition.
38. Petrovich G.D., Canteras N.S., Swanson L.W. Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res. Brain Res. Rev. 2001, 38:247-289.
39. Ray R.S., Corcoran A.E., Brust R.D., Kim J.C., Richerson G.B., Nattie E., Dymecki S.M. Impaired respiratory and body temperature control upon acute serotonergic neuron inhibition. Science 2011, 333:637-642.
40. Roselli C.E. Sex differences in androgen receptors and aromatase activity in microdissected regions of the rat brain. Endocrinology 1991, 128:1310-1316.
41. Roselli C.E., Horton L.E., Resko J.A. Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology 1985, 117:2471-2477.
42. Sasaki K., Suzuki M., Mieda M., Tsujino N., Roth B., Sakurai T. Pharmacogenetic modulation of orexin neurons alters sleep/wakefulness states in mice. PLoS ONE 2011, 6:e20360.
43. Scott J.P. Agonistic behavior of mice and rats: a review. Am. Zool. 1966, 6:683-701.
44. Sokolowski K., Corbin J.G. Wired for behaviors: from development to function of innate limbic system circuitry. Front. Mol. Neurosci. 2012, 5:55.
45. Sternson S.M. Hypothalamic survival circuits: blueprints for purposive behaviors. Neuron 2013, 77:810-824.
46. Sternson S.M., Roth B.L. Chemogenetic tools to interrogate brain functions. Annu. Rev. Neurosci. 2014, 37:387-407.
47. 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 2002, 295:1493-1500.
48. Svare B., Gandelman R. Postpartum aggression in mice: inhibitory effect of estrogen. Physiol. Behav. 1975, 14:31-35.
49. Svare B., Gandelman R. Postpartum aggression in mice: the influence of suckling stimulation. Horm. Behav. 1976, 7:407-416.
50. Svare B., Gandelman R. Suckling stimulation induces aggression in virgin female mice. Nature 1976, 260:606-608.
51. Swanson L.W. Cerebral hemisphere regulation of motivated behavior. Brain Res. 2000, 886:113-164.
52. Swanson L.W., Petrovich G.D. What is the amygdala?. Trends Neurosci. 1998, 21:323-331.
53. Wallis C.J., Luttge W.G. Maintenance of male sexual behavior by combined treatment with oestrogen and dihydrotestosterone in CD-1 mice. J.Endocrinol. 1975, 66:257-262.
54. Wang L., Han X., Mehren J., Hiroi M., Billeter J.-C., Miyamoto T., Amrein H., Levine J.D., Anderson D.J. Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat. Neurosci. 2011, 14:757-762.
55. Wersinger S.R., Sannen K., Villalba C., Lubahn D.B., Rissman E.F., De Vries G.J. Masculine sexual behavior is disrupted in male and female mice lacking a functional estrogen receptor alpha gene. Horm. Behav. 1997, 32:176-183.
56. Wu M.V., Manoli D.S., Fraser E.J., Coats J.K., Tollkuhn J., Honda S., Harada N., Shah N.M. Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 2009, 139:61-72.
57. Wu Z., Autry A.E., Bergan J.F., Watabe-Uchida M., Dulac C.G. Galanin neurons in the medial preoptic area govern parental behaviour. Nature 2014, 509:325-330.
58. Xu X., Coats J.K., Yang C.F., Wang A., Ahmed O.M., Alvarado M., Izumi T., Shah N.M. Modular genetic control of sexually dimorphic behaviors. Cell 2012, 148:596-607.
59. Yang C.F., Shah N.M. Representing sex in the brain, one module at a time. Neuron 2014, 82:261-278.
60. Yang C.F., Chiang M.C., Gray D.C., Prabhakaran M., Alvarado M., Juntti S.A., Unger E.K., Wells J.A., Shah N.M. Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell 2013, 153:896-909.