Lack of spatial segregation in the representation of pheromones and kairomones in the mouse medial amygdala

Frontiers in Neuroscience

Volumn 9, Issue JUL, 2015, Pages

  Carvalho, Vinicius M A ^a   Nakahara, Thiago S ^a   Cardozo, Leonardo M ^a,c   Souza, Mateus A A ^a   Camargo, Antonio P C B R ^a   Trintinalia, Guilherme Z ^a   Ferraz, Eliana ^b   Papes, Fabio ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b Campinas Municipal Zoo   (Brazil)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amygdala; Higher order representation; Olfaction; Pheromone; Vomeronasal organ

Indexed keywords

HORMONE; KAIROMONE; PHEROMONE; PROTEIN C FOS; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; FEMALE; MALE; MEDIAL AMYGDALA; MOUSE; NONHUMAN; ODOR; OLFACTORY SYSTEM; PROTEIN EXPRESSION; SENSORY STIMULATION; SMELLING; VOMERONASAL ORGAN;

EID: 84938387624     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00283     Document Type: Article

References (48)

1. Ben-Shaul, Y., Katz, L. C., Mooney, R., and Dulac, C. (2010). In vivo vomeronasal stimulation reveals sensory encoding of conspecific and allospecific cues by the mouse accessory olfactory bulb. Proc. Natl. Acad. Sci. U. S. A. 107, 5172-5177.
2. Bergan, J. F., Ben-Shaul, Y., and Dulac, C. (2014). Sex-specific processing of social cues in the medial amygdala. Elife 3, e02743.
3. Blanchard, D. C., Canteras, N. S., Markham, C. M., Pentkowski, N. S., and Blanchard, R. J. (2005). Lesions of structures showing FOS expression to cat presentation: Effects on responsivity to a Cat, Cat odor, and nonpredator threat. in Neuroscience and Biobehavioral Reviews, 1243-1253.
4. Canteras, N. S. (2002). The medial hypothalamic defensive system: Hodological organization and functional implications. Pharmacol. Biochem. Behav. 71, 481-491.
5. Canteras, N. S., Chiavegatto, S., Ribeiro do Valle, L. E., and Swanson, L. W. (1997). Severe reduction of rat defensive behavior to a predator by discrete hypothalamic chemical lesions. Brain Res. Bull. 44, 297-305.
6. Canteras, N. S., Simerly, R. B., and Swanson, L. W. (1995). Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat. J. Comp. Neurol. 360, 213-245.
7. Chamero, P., Marton, T. F., Logan, D. W., Flanagan, K., Cruz, J. R., Saghatelian, A., Cravatt, B. F., and Stowers, L. (2007). Identification of protein pheromones that promote aggressive behaviour. Nature 450, 899-902.
8. Chen, X., Gabitto, M., Peng, Y., Ryba, N. J. P., and Zuker, C. S. (2011). A gustotopic map of taste qualities in the mammalian brain. Science 333, 1262-1266.
9. Choi, G. B., Dong, H. W., Murphy, A. J., Valenzuela, D. M., Yancopoulos, G. D., Swanson, L. W., and Anderson, D. J. (2005). Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 46, 647-660.
10. Dey, S., Chamero, P., Pru, J. K., Chien, M.-S., Ibarra-Soria, X., Spencer, K. R., Logan, D. W., Matsunami, H., Peluso, J. J., and Stowers, L. (2015). Cyclic Regulation of Sensory Perception by a Female Hormone Alters Behavior. Cell 161, 1334-1344.
11. Dielenberg, R. A., Hunt, G. E., and McGregor, I. S. (2001). "When a rat smells a cat": The distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience 104, 1085-1097.
12. Dong, H. W., Petrovich, G. D., and Swanson, L. W. (2001). Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Rev. 38, 192-246.
13. Fernandez-Fewell, G. D., and Meredith, M. (1994). c-fos expression in vomeronasal pathways of mated or pheromone-stimulated male golden hamsters: contributions from vomeronasal sensory input and expression related to mating performance. J. Neurosci. 14, 3643-3654.
14. Ferrero, D. M., Moeller, L. M., Osakada, T., Horio, N., Li, Q., Roy, D. S., Cichy, A., Spehr, M., Touhara, K., and Liberles, S. D. (2013). A juvenile mouse pheromone inhibits sexual behaviour through the vomeronasal system. Nature 502, 368-71.
15. Guzowski, J. F., McNaughton, B. L., Barnes, C. A., and Worley, P. F. (1999). Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat. Neurosci. 2, 1120-1124.
16. Guzowski, J. F., McNaughton, B. L., Barnes, C. A., and Worley, P. F. (2001). Imaging neural activity with temporal and cellular resolution using FISH. Curr. Opin. Neurobiol. 11, 579-584.
17. Haga, S., Hattori, T., Sato, T., Sato, K., Matsuda, S., Kobayakawa, R., Sakano, H., Yoshihara, Y., Kikusui, T., and Touhara, K. (2010). The male mouse pheromone ESP1 enhances female sexual receptive behaviour through a specific vomeronasal receptor. Nature 466, 118-122.
18. Hendrickson, R. C., Krauthamer, S., Essenberg, J. M., and Holy, T. E. (2008). Inhibition shapes sex selectivity in the mouse accessory olfactory bulb. J. Neurosci. 28, 12523-12534.
19. Isogai, Y., Si, S., Pont-Lezica, L., Tan, T., Kapoor, V., Murthy, V. N., and Dulac, C. (2011). Molecular organization of vomeronasal chemoreception. Nature 478, 241-5.
20. Kaur, A. W., Ackels, T., Kuo, T. H., Cichy, A., Dey, S., Hays, C., Kateri, M., Logan, D. W., Marton, T. F., Spehr, M., et al. (2014). Murine pheromone proteins constitute a context-dependent combinatorial code governing multiple social behaviors. Cell 157, 676-688.
21. Kimchi, T., Xu, J., and Dulac, C. (2007). A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 448, 1009-14.
22. Kollack-Walker, S., and Newman, S. W. (1997). Mating-induced expression of c-fos in the male Syrian hamster brain: Role of experience, pheromones, and ejaculations. J. Neurobiol. 32, 481-501.
23. Leinders-Zufall, T., Brennan, P., Widmayer, P., S, P. C., Maul-Pavicic, A., Jäger, M., Li, X.-H., Breer, H., Zufall, F., and Boehm, T. (2004). MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306, 1033-7.
24. Lin, D., Boyle, M. P., Dollar, P., Lee, H., Lein, E. S., Perona, P., and Anderson, D. J. (2011). Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221-226.
25. Logan, D. W., Marton, T. F., and Stowers, L. (2008). Species specificity in major urinary proteins by parallel evolution. PLoS One 3.
26. Luo, L., and Flanagan, J. G. (2007). Development of continuous and discrete neural maps. Neuron 56, 284-300.
27. Luo, M., Fee, M. S., and Katz, L. C. (2003). Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 299, 1196-1201.
28. Meredith, M., and Westberry, J. M. (2004). Distinctive responses in the medial amygdala to same species and different-species pheromones. J. Neurosci. 24, 5719-5725.
29. Miyamichi, K., Amat, F., Moussavi, F., Wang, C., Wickersham, I., Wall, N. R., Taniguchi, H., Tasic, B., Huang, Z. J., He, Z., et al. (2011). Cortical representations of olfactory input by trans synaptic tracing. Nature 472, 191-196.
30. Mohedano-Moriano, A., Pro-Sistiaga, P., Úbeda-Bañón, I., Crespo, C., Insausti, R., and Martinez-Marcos, A. (2007). Segregated pathways to the vomeronasal amygdala: Differential projections from the anterior and posterior divisions of the accessory olfactory bulb. Eur. J. Neurosci. 25, 2065-2080.
31. Motta, S. C., Goto, M., Gouveia, F. V, Baldo, M. V. C., Canteras, N. S., and Swanson, L. W. (2009). Dissecting the brain's fear system reveals the hypothalamus is critical for responding in subordinate conspecific intruders. Proc. Natl. Acad. Sci. U. S. A. 106, 4870-4875.
32. Munger, S. D., Leinders-Zufall, T., and Zufall, F. (2009). Subsystem organization of the mammalian sense of smell. Annu. Rev. Physiol. 71, 115-40.
33. Nodari, F., Hsu, F.-F., Fu, X., Holekamp, T. F., Kao, L.-F., Turk, J., and Holy, T. E. (2008). Sulfated steroids as natural ligands of mouse pheromone-sensing neurons. J. Neurosci. 28, 6407-18.
34. Papes, F., Logan, D. W., and Stowers, L. (2010). The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 141, 692-703.
35. Paxinos, G., and Franklin, K. B. J. (2004). The mouse brain in stereotaxic coordinates.
36. Petrovich, G. D., Canteras, N. S., and Swanson, L. W. (2001). Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res. Rev. 38, 247-289.
37. Root, C. M., Denny, C. A., Hen, R., and Axel, R. (2014). The participation of cortical amygdala in innate, odour-driven behaviour. Nature 515, 269-273.
38. Sam, M., Vora, S., Malnic, B., Ma, W., Novotny, M. V, and Buck, L. B. (2001). Neuropharmacology. Odorants may arouse instinctive behaviours. Nature 412, 142.
39. Shakhawat, A. M., Harley, C. W., and Yuan, Q. (2014). Arc visualization of odor objects reveals experience-dependent ensemble sharpening, separation, and merging in anterior piriform cortex in adult rat. J. Neurosci. 34, 10206-10.
40. Silva, B. a, Mattucci, C., Krzywkowski, P., Murana, E., Illarionova, A., Grinevich, V., Canteras, N. S., Ragozzino, D., and Gross, C. T. (2013). Independent hypothalamic circuits for social and predator fear. Nat. Neurosci. 16, 1731-3.
41. Silvotti, L., Moiani, A., Gatti, R., and Tirindelli, R. (2007). Combinatorial co-expression of pheromone receptors, V2Rs. J. Neurochem. 103, 1753-63.
42. Sosulski, D. L., Bloom, M. L., Cutforth, T., Axel, R., and Datta, S. R. (2011). Distinct representations of olfactory information in different cortical centres. Nature 472, 213-216.
43. Stettler, D. D., and Axel, R. (2009). Representations of Odor in the Piriform Cortex. Neuron 63, 854-864.
44. Stowers, L., Holy, T. E., Meister, M., Dulac, C., and Koentges, G. (2002). Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295, 1493-500.
45. Swanson, L. W. (2000). Cerebral hemisphere regulation of motivated behavior. Brain Res. 886, 113-164.
46. Takahashi, L. K. (2014). Olfactory systems and neural circuits that modulate predator odor fear. Front. Behav. Neurosci. 8, 72.
47. Trinh, K., and Storm, D. R. (2003). Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat. Neurosci. 6, 519-25.
48. Wagner, S., Gresser, A. L., Torello, A. T., and Dulac, C. (2006). A Multireceptor Genetic Approach Uncovers an Ordered Integration of VNO Sensory Inputs in the Accessory Olfactory Bulb. Neuron 50, 697-709.