A Bidirectional Circuit Switch Reroutes Pheromone Signals in Male and Female Brains

Overview

Journal Cell

Publisher Cell Press

Specialty Cell Biology

Date 2013 Dec 24

PMID 24360281

Citations 91

Authors

Johannes Kohl

Aaron D Ostrovsky

Shahar Frechter

Gregory S X E Jefferis

Affiliations

Soon will be listed here.

Abstract

The Drosophila sex pheromone cVA elicits different behaviors in males and females. First- and second-order olfactory neurons show identical pheromone responses, suggesting that sex genes differentially wire circuits deeper in the brain. Using in vivo whole-cell electrophysiology, we now show that two clusters of third-order olfactory neurons have dimorphic pheromone responses. One cluster responds in females; the other responds in males. These clusters are present in both sexes and share a common input pathway, but sex-specific wiring reroutes pheromone information. Regulating dendritic position, the fruitless transcription factor both connects the male-responsive cluster and disconnects the female-responsive cluster from pheromone input. Selective masculinization of third-order neurons transforms their morphology and pheromone responses, demonstrating that circuits can be functionally rewired by the cell-autonomous action of a switch gene. This bidirectional switch, analogous to an electrical changeover switch, provides a simple circuit logic to activate different behaviors in males and females.

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References

Jang H, Kim K, Neal S, Macosko E, Kim D, Butcher R . Neuromodulatory state and sex specify alternative behaviors through antagonistic synaptic pathways in C. elegans. Neuron. 2012; 75(4):585-92. PMC: 3462069. DOI: 10.1016/j.neuron.2012.06.034. View

Touhara K, Vosshall L . Sensing odorants and pheromones with chemosensory receptors. Annu Rev Physiol. 2009; 71:307-32. DOI: 10.1146/annurev.physiol.010908.163209. View

Cachero S, Ostrovsky A, Yu J, Dickson B, Jefferis G . Sexual dimorphism in the fly brain. Curr Biol. 2010; 20(18):1589-601. PMC: 2957842. DOI: 10.1016/j.cub.2010.07.045. View

Kimura K, Ote M, Tazawa T, Yamamoto D . Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Nature. 2005; 438(7065):229-33. DOI: 10.1038/nature04229. View

Dickson B . Wired for sex: the neurobiology of Drosophila mating decisions. Science. 2008; 322(5903):904-9. DOI: 10.1126/science.1159276. View

Luan H, Peabody N, Vinson C, White B . Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron. 2006; 52(3):425-36. PMC: 1713190. DOI: 10.1016/j.neuron.2006.08.028. View

Fisek M, Wilson R . Stereotyped connectivity and computations in higher-order olfactory neurons. Nat Neurosci. 2013; 17(2):280-8. PMC: 3992254. DOI: 10.1038/nn.3613. View

Yu J, Kanai M, Demir E, Jefferis G, Dickson B . Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol. 2010; 20(18):1602-14. DOI: 10.1016/j.cub.2010.08.025. View

Tompkins L, Hall J . Identification of Brain Sites Controlling Female Receptivity in Mosaics of DROSOPHILA MELANOGASTER. Genetics. 1983; 103(2):179-95. PMC: 1219973. DOI: 10.1093/genetics/103.2.179. View

10.

Ito H, Sato K, Koganezawa M, Ote M, Matsumoto K, Hama C . Fruitless recruits two antagonistic chromatin factors to establish single-neuron sexual dimorphism. Cell. 2012; 149(6):1327-38. DOI: 10.1016/j.cell.2012.04.025. View

11.

Lee T, Luo L . Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron. 1999; 22(3):451-61. DOI: 10.1016/s0896-6273(00)80701-1. View

12.

Ruta V, Datta S, Vasconcelos M, Freeland J, Looger L, Axel R . A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature. 2010; 468(7324):686-90. DOI: 10.1038/nature09554. View

13.

Rideout E, Dornan A, Neville M, Eadie S, Goodwin S . Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat Neurosci. 2010; 13(4):458-66. PMC: 3092424. DOI: 10.1038/nn.2515. View

14.

White J, Jorgensen E . Sensation in a single neuron pair represses male behavior in hermaphrodites. Neuron. 2012; 75(4):593-600. PMC: 3475325. DOI: 10.1016/j.neuron.2012.03.044. View

15.

Wilson R, Turner G, Laurent G . Transformation of olfactory representations in the Drosophila antennal lobe. Science. 2003; 303(5656):366-70. DOI: 10.1126/science.1090782. View

16.

Wu M, Shah N . Control of masculinization of the brain and behavior. Curr Opin Neurobiol. 2010; 21(1):116-23. PMC: 3046257. DOI: 10.1016/j.conb.2010.09.014. View

17.

Schlief M, Wilson R . Olfactory processing and behavior downstream from highly selective receptor neurons. Nat Neurosci. 2007; 10(5):623-30. PMC: 2838507. DOI: 10.1038/nn1881. View

18.

von Philipsborn A, Liu T, Yu J, Masser C, Bidaye S, Dickson B . Neuronal control of Drosophila courtship song. Neuron. 2011; 69(3):509-22. DOI: 10.1016/j.neuron.2011.01.011. View

19.

Kimchi T, Xu J, Dulac C . A functional circuit underlying male sexual behaviour in the female mouse brain. Nature. 2007; 448(7157):1009-14. DOI: 10.1038/nature06089. View

20.

Wang L, Anderson D . Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature. 2009; 463(7278):227-31. PMC: 2999963. DOI: 10.1038/nature08678. View