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Sensory integration regulating male courtship behavior in Drosophila.

Krstic D, Boll W, Noll M - PLoS ONE (2009)

Bottom Line: By systematic analysis of how variations in sensory inputs alter the courtship behavior of a naïve male in the single-choice courtship paradigm, we derive a model describing the logic of the network that integrates the various sensory stimuli and elicits this complex innate behavior.This approach and the model derived from it distinguish (i) between initiation and maintenance of courtship, (ii) between courtship in daylight and in the dark, where the male uses a scanning strategy to retrieve the decamping female, and (iii) between courtship towards receptive virgin females and mature males.The model will complement studies on the connectivity and intrinsic properties of the neurons forming the circuitry that regulates male courtship behavior.

View Article: PubMed Central - PubMed

Affiliation: Institute for Molecular Biology, University of Zürich, Zürich, Switzerland.

ABSTRACT
The courtship behavior of Drosophila melanogaster serves as an excellent model system to study how complex innate behaviors are controlled by the nervous system. To understand how the underlying neural network controls this behavior, it is not sufficient to unravel its architecture, but also crucial to decipher its logic. By systematic analysis of how variations in sensory inputs alter the courtship behavior of a naïve male in the single-choice courtship paradigm, we derive a model describing the logic of the network that integrates the various sensory stimuli and elicits this complex innate behavior. This approach and the model derived from it distinguish (i) between initiation and maintenance of courtship, (ii) between courtship in daylight and in the dark, where the male uses a scanning strategy to retrieve the decamping female, and (iii) between courtship towards receptive virgin females and mature males. The last distinction demonstrates that sexual orientation of the courting male, in the absence of discriminatory visual cues, depends on the integration of gustatory and behavioral feedback inputs, but not on olfactory signals from the courted animal. The model will complement studies on the connectivity and intrinsic properties of the neurons forming the circuitry that regulates male courtship behavior.

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Vision strongly supports the heterosexual orientation of males.(A) Courtship vigor indices were measured in single-choice courtship assays, performed in the dark or in daylight with courting males of indicated genotypes and decapitated Ore-R virgins (V, filled columns) or decapitated Ore-R males (♂, hatched columns). The number of males that initiated courtship is shown below each column. (B) Fractions of males initiating courtship and (C) average latencies (in seconds) till courtship initiation correspond to the courtship assays in (A) of Ore-R and Poxn-pRes; Or83b2 males courting decapitated flies in daylight.
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pone-0004457-g006: Vision strongly supports the heterosexual orientation of males.(A) Courtship vigor indices were measured in single-choice courtship assays, performed in the dark or in daylight with courting males of indicated genotypes and decapitated Ore-R virgins (V, filled columns) or decapitated Ore-R males (♂, hatched columns). The number of males that initiated courtship is shown below each column. (B) Fractions of males initiating courtship and (C) average latencies (in seconds) till courtship initiation correspond to the courtship assays in (A) of Ore-R and Poxn-pRes; Or83b2 males courting decapitated flies in daylight.

Mentions: In daylight, as in the dark, Ore-R males courted decapitated females very vigorously (Figure 6A). However, when facing a decapitated male in daylight, Ore-R males exhibited a cvi that was substantially reduced compared to that observed in the dark (Figure 6A; p<0.001), which suggested that also visual cues determine the sexual orientation of males. In view of the sexually dimorphic body patterns and sizes of males and females, this conclusion seemed plausible. It was corroborated by the observation that blind ninaB306d males courted decapitated males in daylight with the same cvi as in the dark (M26) (Figure 6A; p = 0.64). The results with ninaB360d males were further supported by courtship assays in daylight with males that could perceive neither gustatory nor olfactory signals. These males could clearly discriminate between decapitated males and females (Poxn-pRes; Or83b2 in Figure 6A; p<0.001), which demonstrates that vision alone is sufficient to enforce heterosexual orientation in single-choice courtship assays (M26). Interestingly, a comparison of courtship initiation towards decapitated males and females in daylight shows that vision does not efficiently prevent Ore-R males from initiating courtship towards decapitated males (Figure 6B,C). Similarly, vision alone stimulates courtship initiation towards both decapitated females (M27) and males (M28) at first (Poxn-pRes; Or83b2 in Figure 6B,C), and it is only after courtship initiation that vision reveals its strong discriminatory property (M26, M29) (Poxn-pRes; Or83b2 in Figure 6A).


Sensory integration regulating male courtship behavior in Drosophila.

Krstic D, Boll W, Noll M - PLoS ONE (2009)

Vision strongly supports the heterosexual orientation of males.(A) Courtship vigor indices were measured in single-choice courtship assays, performed in the dark or in daylight with courting males of indicated genotypes and decapitated Ore-R virgins (V, filled columns) or decapitated Ore-R males (♂, hatched columns). The number of males that initiated courtship is shown below each column. (B) Fractions of males initiating courtship and (C) average latencies (in seconds) till courtship initiation correspond to the courtship assays in (A) of Ore-R and Poxn-pRes; Or83b2 males courting decapitated flies in daylight.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2636894&req=5

pone-0004457-g006: Vision strongly supports the heterosexual orientation of males.(A) Courtship vigor indices were measured in single-choice courtship assays, performed in the dark or in daylight with courting males of indicated genotypes and decapitated Ore-R virgins (V, filled columns) or decapitated Ore-R males (♂, hatched columns). The number of males that initiated courtship is shown below each column. (B) Fractions of males initiating courtship and (C) average latencies (in seconds) till courtship initiation correspond to the courtship assays in (A) of Ore-R and Poxn-pRes; Or83b2 males courting decapitated flies in daylight.
Mentions: In daylight, as in the dark, Ore-R males courted decapitated females very vigorously (Figure 6A). However, when facing a decapitated male in daylight, Ore-R males exhibited a cvi that was substantially reduced compared to that observed in the dark (Figure 6A; p<0.001), which suggested that also visual cues determine the sexual orientation of males. In view of the sexually dimorphic body patterns and sizes of males and females, this conclusion seemed plausible. It was corroborated by the observation that blind ninaB306d males courted decapitated males in daylight with the same cvi as in the dark (M26) (Figure 6A; p = 0.64). The results with ninaB360d males were further supported by courtship assays in daylight with males that could perceive neither gustatory nor olfactory signals. These males could clearly discriminate between decapitated males and females (Poxn-pRes; Or83b2 in Figure 6A; p<0.001), which demonstrates that vision alone is sufficient to enforce heterosexual orientation in single-choice courtship assays (M26). Interestingly, a comparison of courtship initiation towards decapitated males and females in daylight shows that vision does not efficiently prevent Ore-R males from initiating courtship towards decapitated males (Figure 6B,C). Similarly, vision alone stimulates courtship initiation towards both decapitated females (M27) and males (M28) at first (Poxn-pRes; Or83b2 in Figure 6B,C), and it is only after courtship initiation that vision reveals its strong discriminatory property (M26, M29) (Poxn-pRes; Or83b2 in Figure 6A).

Bottom Line: By systematic analysis of how variations in sensory inputs alter the courtship behavior of a naïve male in the single-choice courtship paradigm, we derive a model describing the logic of the network that integrates the various sensory stimuli and elicits this complex innate behavior.This approach and the model derived from it distinguish (i) between initiation and maintenance of courtship, (ii) between courtship in daylight and in the dark, where the male uses a scanning strategy to retrieve the decamping female, and (iii) between courtship towards receptive virgin females and mature males.The model will complement studies on the connectivity and intrinsic properties of the neurons forming the circuitry that regulates male courtship behavior.

View Article: PubMed Central - PubMed

Affiliation: Institute for Molecular Biology, University of Zürich, Zürich, Switzerland.

ABSTRACT
The courtship behavior of Drosophila melanogaster serves as an excellent model system to study how complex innate behaviors are controlled by the nervous system. To understand how the underlying neural network controls this behavior, it is not sufficient to unravel its architecture, but also crucial to decipher its logic. By systematic analysis of how variations in sensory inputs alter the courtship behavior of a naïve male in the single-choice courtship paradigm, we derive a model describing the logic of the network that integrates the various sensory stimuli and elicits this complex innate behavior. This approach and the model derived from it distinguish (i) between initiation and maintenance of courtship, (ii) between courtship in daylight and in the dark, where the male uses a scanning strategy to retrieve the decamping female, and (iii) between courtship towards receptive virgin females and mature males. The last distinction demonstrates that sexual orientation of the courting male, in the absence of discriminatory visual cues, depends on the integration of gustatory and behavioral feedback inputs, but not on olfactory signals from the courted animal. The model will complement studies on the connectivity and intrinsic properties of the neurons forming the circuitry that regulates male courtship behavior.

Show MeSH
Related in: MedlinePlus