Scalable control of mounting and attack by Esr1+ neurons in the ventromedial hypothalamus

Nature

Volumn 509, Issue 7502, 2014, Pages 627-632

  Lee, Hyosang ^a,b   Kim, Dong Wook ^c   Remedios, Ryan ^a   Anthony, Todd E ^a   Chang, Angela ^a   Madisen, Linda ^d   Zeng, Hongkui ^d   Anderson, David J ^a,b,c  

^a California Institute of Technology   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^d ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; ESTROGEN RECEPTOR ALPHA;

AGGRESSION; DATA SET; INHIBITION; MATING BEHAVIOR; NEUROLOGY; SOCIAL BEHAVIOR;

ADULT; AGGRESSION; ANIMAL CELL; ANIMAL EXPERIMENT; AROUSAL; ARTICLE; CONTROLLED STUDY; EMBRYONIC STEM CELL; FEMALE; MALE; MATING; MOUSE; NERVE CELL; NONHUMAN; ONCOGENE C FOS; OPTOGENETICS; PHENOTYPE; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY STIMULATION; SOCIAL BEHAVIOR; SOCIAL INTERACTION; WHOLE CELL PATCH CLAMP; ZONA INCERTA;

MURINAE;

AGGRESSION; ANIMALS; ESTROGEN RECEPTOR ALPHA; FEMALE; INTEGRASES; MALE; MICE; NEURONS; OPTOGENETICS; SEXUAL BEHAVIOR, ANIMAL; VENTROMEDIAL HYPOTHALAMIC NUCLEUS;

EID: 84901660911     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13169     Document Type: Article

References (41)

1. Tinbergen, N. in Physiological Mechanisms in Animal Behaviour Vol. IV Symposia of the Society for Experimental Biology 305-312 (Academic Press, 1950).
2. 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).
3. Lin, D. et al. Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221-226 (2011).
4. Lein, E. S. et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168-176 (2007).
5. Morgan, J. I., Cohen, D. R., Hempstead, J. L. & Curran, T. Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237, 192-197 (1987).
6. Walter, P. et al. Cloning of the human estrogen receptor cDNA. Proc. Natl Acad. Sci. USA 82, 7889-7893 (1985).
7. Xu, X. et al. Modular genetic control of sexually dimorphic behaviors. Cell 148, 596-607 (2012).
8. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Milli second time scale, genetically targeted optical control of neural activity. Nature Neurosci. 8, 1263-1268 (2005).
9. Aravanis, A. M. et al. An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. J. Neural Eng. 4, S143-S156 (2007).
10. Blanchard, D. C. & Blanchard, R. J. Ethoexperimental approaches to the biology of emotion. Annu. Rev. Psychol. 39, 43-68 (1988).
11. 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).
12. Sano, K., Tsuda, M. C., Musatov, S., Sakamoto, T. & Ogawa, S. Differential effects of site-specific knockdown of estrogen receptor alpha 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).
13. Gradinaru, V. et al. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141, 154-165 (2010).
14. Blanchard, R. J., Wall, P. M. & Blanchard, D. C. Problems in the study of rodent aggression. Horm. Behav. 44, 161-170 (2003).
15. Chen, T. W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
16. 2 channel. Neuron 54, 35-49 (2007).
17. Cohen, R. S. & Pfaff, D. W. Ventromedial hypothalamic neurons in the mediation of long-lasting effects of estrogen on lordosis behavior. Prog. Neurobiol. 38, 423-453 (1992).
18. Musatov, S., Chen, W., Pfaff, D. W., Kaplitt, M. G. & Ogawa, S. RNAi-mediated silencing of estrogen receptor a in the ventromedial nucleus of hypothalamus abolishes female sexual behaviors. Proc. Natl Acad. Sci. USA 103, 10456-10460 (2006).
19. Spiteri, T. et al. Estrogen-induced sexual incentive motivation, proceptivity and receptivity depend on a functional estrogen receptor alpha in the ventromedial nucleus of the hypothalamus but not in the amygdala. Neuroendocrinology 91, 142-154 (2010).
20. Spiteri, T. et al. The role of the estrogen receptor alpha in the medialamygdala and ventromedial nucleus of the hypothalamus in social recognition, anxiety and aggression. Behav. Brain Res. 210, 211-220 (2010).
21. Simerly, R. B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci. 25, 507-536 (2002).
22. Morris, J. A., Jordan, C. L. & Breedlove, S. M. Sexual differentiation of the vertebrate nervous system. Nature Neurosci. 7, 1034-1039 (2004).
23. Wu, M. V. & Shah, N. M. Control of masculinization of the brain and behavior. Curr. Opin. Neurobiol. 21, 116-123 (2011).
24. Kow, L. M., Easton, A. & Pfaff, D. W. Acute estrogen potentiates excitatory responses of neurons in rat hypothalamic ventromedial nucleus. Brain Res. 10, 124-131 (2005).
25. Bentley, D. & Konishi, M. Neural control of behavior. Annu. Rev. Neurosci. 1, 35-59 (1978).
26. 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).
27. Anderson, D. J. Optogenetics, sex, and violence in the brain: implications for psychiatry. Biol. Psychiatry 71, 1081-1089 (2011).
28. Kristan, W. B. Neuronal decision-making circuits. Curr. Biol. 18, R928-R932 (2008).
29. Haubensak, W. et al. Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468, 270-276 (2010).
30. Vrontou, S., Wong, A. M., Rau, K. K., Koerber, H. R. & Anderson, D. J. Genetic identification of C fibres that detect massage-like stroking of hairy skin in vivo. Nature 493, 669-673 (2013).
31. Wu, Y., Wang, C., Sun, H., LeRoith, D. & Yakar, S. High-efficient FLPo deleter mice in C57BL/6J background. PLoS ONE 4, e8054 (2009).
32. Lin, D. et al. Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221-226 (2011).
33. Harris, J. A., Oh, S. W. & Zeng, H. Adeno-associated viral vectors for anterograde axonal tracing with fluorescent proteins in nontransgenic and cre driver mice. Curr Protoc Neurosci Chapter 1, Unit 1 20 21-18 (2012).
34. Chan, E., Kovacevic, N., Ho, S. K., Henkelman, R. M. & Henderson, J. T. Development of a high resolution three-dimensional surgical atlas of the murine head for strains 129S1/SvImJ and C57Bl/6J using magnetic resonance imaging and microcomputed tomography. Neuroscience 144, 604-615 (2007).
35. Lein, E. S. et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168-176 (2007).
36. Haubensak, W. et al. Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468, 270-276 (2010).
37. Atasoy, D., Betley, J. N., Su, H. H. & Sternson, S. M. Deconstruction of a neural circuit for hunger. Nature 488, 172-177 (2012).
38. Chen, T. W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
39. Vrontou, S., Wong, A. M., Rau, K. K., Koerber, H. R. & Anderson, D. J. Genetic identification of C fibres that detect massage-like stroking of hairy skin in vivo. Nature 493, 669-673 (2013).
40. Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B. & Uchida, N. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482, 85-88 (2012).
41. Kvitsiani, D. et al. Distinct behavioural and network correlates of two interneuron types in prefrontal cortex. Nature 498, 363-366 (2013).