Doublesex Regulates the Connectivity of a Neural Circuit Controlling Drosophila Male Courtship Song

Shirangi, Troy R.; Wong, Allan; Truman, James W.; Stern, David L.

doi:10.1016/j.devcel.2016.05.012

Cited by 97 publications

(145 citation statements)

References 47 publications

(65 reference statements)

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“…Therefore, there is no evidence that the data resulting from the song segmenter parameters used in Stern (2) generated a dataset that was biased against detection of song rhythms. While the song segmenter does not detect all pulse events that can be detected by manual annotation, the segmenter does provide datasets that are several orders of magnitude larger than those that can be generated by manual annotation, which has allowed discovery of multiple new phenomena related to Drosophila courtship song (3)(4)(5)(6)(7). In addition, the sensitivity of the song segmenter can be improved with optimization of initial parameters, as expected of any segmentation algorithm.…”

Section: No Evidence That the Automated Fly Song Segmenter Biased Thementioning

confidence: 99%

“…1A). Every parameter of song displays extensive quantitative variation within a bout of singing, including the amplitude and frequency of pulses and sines and the timing of individual pulse and sine events (1)(2)(3)(4)(5)(6)(7)(8). Like humans during conversation, Drosophila males modulate their song based on sensory feedback from their communication partner (3,4).…”

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confidence: 99%

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Experimental and statistical reevaluation provides no evidence forDrosophilacourtship song rhythms

Stern¹,

Clemens²,

Coen³

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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From 1980 to 1992, a series of influential papers reported on the discovery, genetics, and evolution of a periodic cycling of the interval between Drosophila male courtship song pulses. The molecular mechanisms underlying this periodicity were never described. To reinitiate investigation of this phenomenon, we previously performed automated segmentation of songs but failed to detect the proposed rhythm [Arthur BJ, et al. (2013) BMC Biol 11:11; Stern DL (2014) BMC Biol 12:38]. Kyriacou et al. [Kyriacou CP, et al. (2017) Proc Natl Acad Sci USA 114:1970-1975] report that we failed to detect song rhythms because (i) our flies did not sing enough and (ii) our segmenter did not identify many of the song pulses. Kyriacou et al. manually annotated a subset of our recordings and reported that two strains displayed rhythms with genotype-specific periodicity, in agreement with their original reports. We cannot replicate this finding and show that the manually annotated data, the original automatically segmented data, and a new dataset provide no evidence for either the existence of song rhythms or song periodicity differences between genotypes. Furthermore, we have reexamined our methods and analysis and find that our automated segmentation method was not biased to prevent detection of putative song periodicity. We conclude that there is no evidence for the existence of Drosophila courtship song rhythms.Drosophila | courtship song | song rhythms W hen a male vinegar fly (Drosophila melanogaster) encounters a sexually receptive female, he performs a series of courtship behaviors, including the production of songs containing pulses and hums (or sines) via unilateral wing vibration (Fig. 1A). Every parameter of song displays extensive quantitative variation within a bout of singing, including the amplitude and frequency of pulses and sines and the timing of individual pulse and sine events (1-8). Like humans during conversation, Drosophila males modulate their song based on sensory feedback from their communication partner (3, 4).Visual inspection of songs reveals that the mean interpulse interval varies over time (Fig. 1B). This observation was first made in 1980 by Kyriacou and Hall (9) and they reported that the mean cycled with a periodicity of about 55 s and was controlled, in part, by the period gene, a gene required for circadian rhythms (10). Later papers demonstrated that evolution of a short amino acid sequence within the period protein caused species-specific differences in this periodicity (10-13). These reports attracted considerable interest because they implicated the period gene in ultradian rhythms, in addition to its well-known role in circadian rhythms (14), and because they illustrated how genetic evolution can cause behavioral evolution.Despite this progress, the molecular mechanisms causing this periodicity remained unknown. To further advance study of these rhythms, previously we searched for this periodicity using sensitive methods and failed to find evidence for song rhythms (1). We were mindful, how...

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Section: No Evidence That the Automated Fly Song Segmenter Biased Thementioning

confidence: 99%

mentioning

confidence: 99%

Experimental and statistical reevaluation provides no evidence forDrosophilacourtship song rhythms

Stern¹,

Clemens²,

Coen³

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Furthermore, quantifying pulse-song intensity is also unlikely to be reliable, because the automated software ignores so much low-intensity pulse song. Indeed any measure that includes pulse song as a variable needs to be reexamined manually (40)(41)(42).…”

Section: Discussionmentioning

confidence: 99%

Failure to reproduce period -dependent song cycles in Drosophila is due to poor automated pulse-detection and low-intensity courtship

Kyriacou

Green

Piffer

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Stern has criticized a body of work from several groups that have independently studied the so-called "Kyriacou and Hall" courtship song rhythms of male Drosophila melanogaster, claiming that these ultradian ∼60-s cycles in the interpulse interval (IPI) are statistical artifacts that are not modulated by mutations at the period (per) locus [Stern DL (2014) BMC Biol 12:38]. We have scrutinized Stern's raw data and observe that his automated song pulse-detection method identifies only ∼50% of the IPIs found by manual (visual and acoustic) monitoring. This critical error is further compounded by Stern's use of recordings with very little song, the large majority of which do not meet the minimal song intensity criteria which Kyriacou and Hall used in their studies. Consequently most of Stern's recordings only contribute noise to the analyses. Of the data presented by Stern, only per L and a small fraction of wild-type males sing vigorously, so we limited our reanalyses to these genotypes. We manually reexamined Stern's raw song recordings and analyzed IPI rhythms using several independent time-series analyses. We observe that per L songs show significantly longer song periods than wildtype songs, with values for both genotypes close to those found in previous studies. These per-dependent differences disappear when the song data are randomized. We conclude that Stern's negative findings are artifacts of his inadequate pulse-detection methodology coupled to his use of low-intensity courtship song records.D uring courtship, the Drosophila melanogaster male vibrates his wing toward the female and produces a series of pulses and hums (1). The pulses have a variable interpulse interval (IPI), which ranges from 15 to 80 ms but usually averages between 30 and 40 ms, whereas sympatric Drosophila simulans mean IPIs vary from 45 to 80 ms depending on the strain (2, 3). In 1980, in these pages, the first of a series of studies by Kyriacou, Hall, and their collaborators revealed that superimposed on these IPIs was a low-amplitude oscillation of about 60 s in D. melanogaster and 40 s in D. simulans (4-12). Furthermore, in D. melanogaster, these cycles were modulated in a predictable fashion by the circadian rhythm period (per) mutations (13): per L males with long 29-h circadian cycles also sang with long ∼80-s song cycles, whereas circadian arrhythmic per 01 males showed a corresponding song phenotype (2, 4, 9, 10). These cycles were shown to have functional significance in playback experiments in which females were shown to be most responsive to both their species-specific IPI and cycle (2, 14-16).The work of Kyriacou, Hall, and collaborators was performed in the late 1970s and 1980s using extremely laborious analog technology, so to attain any kind of throughput, IPIs were binned into consecutive 10-s intervals and a mean IPI calculated on a minimum of 10 IPIs (2, 4-6, 8). Initially, sine/cosine functions were fitted to the mean IPIs (2, 4-6, 8), and this was later complemented by spectral analyses, with both types of statisti...

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“…The upstream neuron is then optogenetically activated while the downstream neuron expressing GCaMP6 is monitored for changes in fluorescence (Figure 6c). These experiments can be done with the nervous system kept in the body or using a dissected brain (Kallman et al 2015;Zhou et al 2015;Clowney et al 2015;Hampel et al 2015;Cohn et al 2015;Shirangi et al 2016). The functional connectivity between neurons that is demonstrated by measuring GECI responses cannot indicate whether the connections are direct, and it is always possible that intermediate neurons are involved.…”

Section: Assessing Functional Connectivity Among Neuronsmentioning

confidence: 99%

Targeted manipulation of neuronal activity in behaving adult flies

Hampel

Seeds

2016

Preprint

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The ability to control the activity of specific neurons in freely behaving animals provides an effective way to probe the contributions of neural circuits to behavior. Wide interest in studying principles of neural circuit function using the fruit fly Drosophila melanogaster has fueled the construction of an extensive transgenic toolkit for performing such neural manipulations. Here we describe approaches for using these tools to manipulate the activity of specific neurons and assess how those manipulations impact the behavior of flies. We also describe methods for examining connectivity among multiple neurons that together form a neural circuit controlling a specific behavior. This work provides a resource ABSTRACTThe ability to control the activity of specific neurons in freely behaving animals provides an effective way to probe the contributions of neural circuits to behavior. Wide interest in studying principles of neural circuit function using the fruit fly Drosophila melanogaster has fueled the construction of an extensive transgenic toolkit for performing such neural manipulations. Here we describe approaches for using these tools to manipulate the activity of specific neurons and assess how those manipulations impact the behavior of flies. We also describe methods for examining connectivity among multiple neurons that together form a neural circuit controlling a specific behavior. This work provides a resource for researchers interested in examining how neurons and neural circuits contribute to the rich repertoire of behaviors performed by flies.

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Doublesex Regulates the Connectivity of a Neural Circuit Controlling Drosophila Male Courtship Song

Cited by 97 publications

References 47 publications

Experimental and statistical reevaluation provides no evidence forDrosophilacourtship song rhythms

Experimental and statistical reevaluation provides no evidence forDrosophilacourtship song rhythms

Failure to reproduce period -dependent song cycles in Drosophila is due to poor automated pulse-detection and low-intensity courtship

Targeted manipulation of neuronal activity in behaving adult flies

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