Medial preoptic area in mice is capable of mediating sexually dimorphic behaviors regardless of gender

Nature Communications

Volumn 9, Issue 1, 2018, Pages

  Wei, Yi Chao ^a,b   Wang, Shao Ran ^a,b   Jiao, Zhuo Lei ^a,b   Zhang, Wen ^a   Lin, Jun Kai ^a,b   Li, Xing Yu ^a,b   Li, Shuai Shuai ^a,b   Zhang, Xin ^a   Xu, Xiao Hong ^a  

^a Shenzhen Fundamental Research Institutions   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; ESTROGEN RECEPTOR ALPHA; PROTEIN C FOS;

BEHAVIORAL RESPONSE; BRAIN; GENDER; INHIBITION; RODENT; SEXUAL BEHAVIOR; SEXUAL DIMORPHISM;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CALCIUM TRANSPORT; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; FLUORESCENCE; IMMUNOHISTOCHEMISTRY; MALE; MEDIAL PREOPTIC AREA; MOUSE; NONHUMAN; OPTOGENETICS; PHOTOMETRY; PHOTOSTIMULATION; PROTEIN EXPRESSION; SEX DIFFERENCE; SOCIAL BEHAVIOR; SOCIAL INTERACTION; ANIMAL; BRAIN; C57BL MOUSE; HUMAN; METABOLISM; NERVE CELL; PHYSIOLOGY; PREOPTIC AREA; PROCEDURES; SEX FACTOR; SEXUAL BEHAVIOR; TRANSGENIC MOUSE;

MUS;

ANIMALS; BRAIN; ESTROGEN RECEPTOR ALPHA; FEMALE; HUMANS; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; OPTOGENETICS; PREOPTIC AREA; SEX FACTORS; SEXUAL BEHAVIOR, ANIMAL;

EID: 85040782472     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-02648-0     Document Type: Article

References (68)

1. Kelley, D. B. Sexually dimorphic behaviors. Annu. Rev. Neurosci. 11, 225-251 (1988).
2. Ruta, V. et al. A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 468, 686-690 (2010).
3. Oren-Suissa, M., Bayer, E. A. & Hobert, O. Sex-specific pruning of neuronal synapses in Caenorhabditis elegans. Nature 533, 206-211 (2016).
4. Simerly, R. B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci. 25, 507-536 (2002).
5. Yang, C. F. & Shah, N. M. Representing sex in the brain, one module at a time. Neuron 82, 261-278 (2014).
6. Sakuma, Y. Gonadal steroid action and brain sex differentiation in the rat. J. Neuroendocrinol. 21, 410-414 (2009).
7. Orikasa, C. & Sakuma, Y. Estrogen configures sexual dimorphism in the preoptic area of C57BL/6J and ddN strains of mice. J. Comp. Neurol. 518, 3618-3629 (2010).
8. Xu, X. et al. Modular genetic control of sexually dimorphic behaviors. Cell 148, 596-607 (2012).
9. Ruigrok, A. N. V. et al. A meta-analysis of sex differences in human brain structure. Neurosci. Biobehav. Rev. 39, 34-50 (2014).
10. Jazin, E. & Cahill, L. Sex differences in molecular neuroscience: from fruit flies to humans. Nat. Rev. Neurosci. 11, 9-17 (2010).
11. Block, A., Ahmed, M. M., Dhanasekaran, A. R., Tong, S. & Gardiner, K. J. Sex differences in protein expression in the mouse brain and their perturbations in a model of Down syndrome. Biol. Sex Differ. 6, 24 (2015).
12. Ingalhalikar, M. et al. Sex differences in the structural connectome of the human brain. Proc. Natl Acad. Sci. USA 111, 823-828 (2014).
13. Lenz, K. M., Nugent, B. M. & McCarthy, M. M. Sexual differentiation of the rodent brain: dogma and beyond. Front. Neurosci. 6, 26 (2012).
14. Nugent, B. M. et al. Brain feminization requires active repression of masculinization via DNA methylation. Nat. Neurosci. 18, 690-697 (2015).
15. McCarthy, M. M. et al. The epigenetics of sex differences in the brain. J. Neurosci. 29, 12815-12823 (2009).
16. 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 509, 325-330 (2014).
17. McHenry, J. A. et al. Hormonal gain control of a medial preoptic area social reward circuit. Nat. Neurosci. 20, 449-458 (2017).
18. O'Connell, L. A. & Hofmann, H. A. Evolution of a vertebrate social decision-making network. Science 336, 1154-1157 (2012).
19. Newman, S. W. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann. N. Y. Acad. Sci. 877, 242-257 (1999).
20. Tsuneoka, Y. et al. Functional, anatomical, and neurochemical differentiation of medial preoptic area subregions in relation to maternal behavior in the mouse. J. Comp. Neurol. 521, 1633-1663 (2013).
21. Swaab, D. F. & Fliers, E. A sexually dimorphic nucleus in the human brain. Science 228, 1112-1115 (1985).
22. Hofman, M. A. & Swaab, D. F. The sexually dimorphic nucleus of the preoptic area in the human brain: a comparative morphometric study. J. Anat. 164, 55-72 (1989).
23. Allen, L. S., Hines, M., Shryne, J. E. & Gorski, R. A. Two sexually dimorphic cell groups in the human brain. J. Neurosci. 9, 497-506 (1989).
24. Tsukahara, S., Kanaya, M. & Yamanouchi, K. Neuroanatomy and sex differences of the lordosis-inhibiting system in the lateral septum. Front. Neurosci. 8, 299 (2014).
25. Simerly, R. B. & Swanson, L. W. The organization of neural inputs to the medial preoptic nucleus of the rat. J. Comp. Neurol. 246, 312-342 (1986).
26. Gu, G., Cornea, A. & Simerly, R. B. Sexual differentiation of projections from the principal nucleus of the bed nuclei of the stria terminalis. J. Comp. Neurol. 460, 542-562 (2003).
27. Canteras, N. S., Simerly, R. B. & Swanson, L. W. Projections of the ventral premammillary nucleus. J. Comp. Neurol. 324, 195-212 (1992).
28. Gorski, R. A., Harlan, R. E., Jacobson, C. D., Shryne, J. E. & Southam, A. M. Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat. J. Comp. Neurol. 193, 529-539 (1980).
29. Sickel, M. J. & McCarthy, M. M. Calbindin-D28k immunoreactivity is a marker for a subdivision of the sexually dimorphic nucleus of the preoptic area of the rat: developmental profile and gonadal steroid modulation. J. Neuroendocrinol. 12, 397-402 (2000).
30. Campi, K. L., Jameson, C. E. & Trainor, B. C. Sexual dimorphism in the brain of the monogamous california mouse (Peromyscus californicus). Brain Behav. Evol. 81, 236-249 (2013).
31. Panzica, G. C., Viglietti-Panzica, C. & Balthazart, J. The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on male sexual behavior. Front. Neuroendocrinol. 17, 51-125 (1996).
32. Raisman, G. & Field, P. M. Sexual dimorphism in the neuropil of the preoptic area of the rat and its dependence on neonatal androgen. Brain Res. 54, 1-29 (1973).
33. Raisman, G. & Field, P. M. Sexual dimorphism in the preoptic area of the rat. Science 173, 731-733 (1971).
34. Ayoub, D. M., Greenough, W. T. & Juraska, J. M. Sex differences in dendritic structure in the preoptic area of the juvenile macaque monkey brain. Science 219, 197-198 (1983).
35. Simerly, R. B., Swanson, L. W. & Gorski, R. A. Demonstration of a sexual dimorphism in the distribution of serotonin-immunoreactive fibers in the medial preoptic nucleus of the rat. J. Comp. Neurol. 225, 151-166 (1984).
36. Simerly, R. B., Swanson, L. W. & Gorski, R. A. Reversal of the sexually dimorphic distribution of serotonin-immunoreactive fibers in the medial preoptic nucleus by treatment with perinatal androgen. Brain Res. 340, 91-98 (1985).
37. De Vries, G. J. & Boyle, P. A. Double duty for sex differences in the brain. Behav. Brain Res. 92, 205-213 (1998).
38. Lin, D. et al. Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221-226 (2011).
39. Hart, B. L., Haugen, C. M. & Peterson, D. M. Effects of medial preoptic-anterior hypothalamic lesions of mating behavior of male cats. Brain Res. 54, 177-191 (1973).
40. Swann, J. M., Wang, J. & Govek, E. K. The MPN mag: introducing a critical area mediating pheromonal and hormonal regulation of male sexual behavior. Ann. N. Y. Acad. Sci. 1007, 199-210 (2003).
41. Slimp, J. C., Hart, B. L. & Goy, R. W. Heterosexual, autosexual and social behavior of adult male rhesus monkeys with medial preoptic-anterior hypothalamic lesions. Brain Res. 142, 105-122 (1978).
42. Marques, D. M., Malsbury, C. W. & Daood, J. Hypothalamic knife cuts dissociate maternal behaviors, sexual receptivity, and estrous cyclicity in female hamsters. Physiol. Behav. 23, 347-355 (1979).
43. Slawski, B. A. & Buntin, J. D. Preoptic area lesions disrupt prolactin-induced parental feeding behavior in ring doves. Horm. Behav. 29, 248-266 (1995).
44. Numan, M. Medial preoptic area and maternal behavior in the female rat. J. Comp. Physiol. Psychol. 87, 746-759 (1974).
45. Perrin, G., Meurisse, M. & Lévy, F. Inactivation of the medial preoptic area or the bed nucleus of the stria terminalis differentially disrupts maternal behavior in sheep. Horm. Behav. 52, 461-473 (2007).
46. Wu, M. V. et al. Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 139, 61-72 (2009).
47. Kimchi, T., Xu, J. & Dulac, C. A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 448, 1009-1014 (2007).
48. Chen, T.-W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
49. Gunaydin, L. A. et al. Natural neural projection dynamics underlying social behavior. Cell 157, 1535-1551 (2014).
50. Li, Y. et al. Serotonin neurons in the dorsal raphe nucleus encode reward signals. Nat. Commun. 7, 10503 (2016).
51. Zhang, F., Wang, L.-P., Boyden, E. S. & Deisseroth, K. Channelrhodopsin-2 and optical control of excitable cells. Nat. Methods 3, 785-792 (2006).
52. The Neurobiology of Parental Behavior | Michael Numan | Springer. Available at: http://www.springer.com/us/book/9780387004983 (accessed 17 October 2017).
53. Lee, H. et al. Scalable control of mounting and attack by Esr1+neurons in the ventromedial hypothalamus. Nature 509, 627-632 (2014).
54. 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).
55. Wu, Q., Howell, M. P. & Palmiter, R. D. Ablation of neurons expressing agouti-related protein activates fos and gliosis in postsynaptic target regions. J. Neurosci. 28, 9218-9226 (2008).
56. Govorunova, E. G., Sineshchekov, O. A., Janz, R., Liu, X. & Spudich, J. L. NEUROSCIENCE. Natural light-gated anion channels: a family of microbial rhodopsins for advanced optogenetics. Science 349, 647-650 (2015).
57. Rezával, C. et al. Activation of latent courtship circuitry in the brain of drosophila females induces male-like behaviors. Curr. Biol. 26, 2508-2515 (2016).
58. Clyne, J. D. & Miesenböck, G. Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133, 354-363 (2008).
59. Zhao, Z.-D. et al. A hypothalamic circuit that controls body temperature. Proc. Natl Acad. Sci. USA 114, 2042-2047 (2017).
60. Chung, S. et al. Identification of preoptic sleep neurons using retrograde labelling and gene profiling. Nature 545, 477-481 (2017).
61. Scott, N., Prigge, M., Yizhar, O. & Kimchi, T. A sexually dimorphic hypothalamic circuit controls maternal care and oxytocin secretion. Nature 525, 519-522 (2015).
62. Flusberg, B. A. et al. High-speed, miniaturized fluorescence microscopy in freely moving mice. Nat. Methods 5, 935-938 (2008).
63. Sakurai, K. et al. Capturing and manipulating activated neuronal ensembles with CANE delineates a hypothalamic social-fear circuit. Neuron 92, 739-753 (2016).
64. Sørensen, A. T. et al. A robust activity marking system for exploring active neuronal ensembles. eLife 5, e13918 (2016).
65. Tervo, D. G. R. et al. A designer AAV variant permits efficient retrograde access to projection neurons. Neuron 92, 372-382 (2016).
66. Zingg, B. et al. AAV-mediated anterograde transsynaptic tagging: mapping corticocollicular input-defined neural pathways for defense behaviors. Neuron 93, 33-47 (2017).
67. Chen, R., Wu, X., Jiang, L. & Zhang, Y. Single-cell RNA-seq reveals hypothalamic cell diversity. Cell Rep. 18, 3227-3241 (2017).
68. Chao, H.-T. et al. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468, 263-269 (2010).