fruitless tunes functional flexibility of courtship circuitry during development

Abstract

Drosophila male courtship is controlled by the male-specific products of the fruitless (fruM) gene and its expressing neuronal circuitry. fruM is considered a master gene that controls all aspects of male courtship. By temporally and spatially manipulating fruM expression, we found that fruM is required during a critical developmental period for innate courtship towards females, while its function during adulthood is involved in inhibiting male-male courtship. By altering or eliminating fruM expression, we generated males that are innately heterosexual, homosexual, bisexual, or without innate courtship but could acquire such behavior in an experience-dependent manner. These findings show that fruM is not absolutely necessary for courtship but is critical during development to build a sex circuitry with reduced flexibility and enhanced efficiency, and provide a new view about how fruM tunes functional flexibility of a sex circuitry instead of switching on its function as conventionally viewed.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1, 2, 3, Figure 3-figure supplement 1, 2 and 4.

Article and author information

Author details

  1. Jie Chen

    School of Life Science and Technology, Southeast University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Sihui Jin

    School of Life Science and Technology, Southeast University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Dandan Chen

    School of Life Science and Technology, Southeast University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Jie Cao

    School of Life Science and Technology, Southeast University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Xiaoxiao Ji

    School of Life Science and Technology, Southeast University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Qionglin Peng

    School of Life Science and Technology, Southeast University, Nanjing, China
    For correspondence
    pengqionglin@seu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  7. Yufeng Pan

    School of Life Science and Technology, Southeast University, Nanjing, China
    For correspondence
    pany@seu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1535-9716

Funding

National Natural Science Foundation of China (31970943,31622028)

  • Yufeng Pan

National Natural Science Foundation of China (31700905)

  • Qionglin Peng

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2021, Chen et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 3,224
    views
  • 539
    downloads
  • 17
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Jie Chen
  2. Sihui Jin
  3. Dandan Chen
  4. Jie Cao
  5. Xiaoxiao Ji
  6. Qionglin Peng
  7. Yufeng Pan
(2021)
fruitless tunes functional flexibility of courtship circuitry during development
eLife 10:e59224.
https://doi.org/10.7554/eLife.59224

Share this article

https://doi.org/10.7554/eLife.59224

Further reading

    1. Neuroscience
    Paul I Jaffe, Gustavo X Santiago-Reyes ... Russell A Poldrack
    Research Article

    Evidence accumulation models (EAMs) are the dominant framework for modeling response time (RT) data from speeded decision-making tasks. While providing a good quantitative description of RT data in terms of abstract perceptual representations, EAMs do not explain how the visual system extracts these representations in the first place. To address this limitation, we introduce the visual accumulator model (VAM), in which convolutional neural network models of visual processing and traditional EAMs are jointly fitted to trial-level RTs and raw (pixel-space) visual stimuli from individual subjects in a unified Bayesian framework. Models fitted to large-scale cognitive training data from a stylized flanker task captured individual differences in congruency effects, RTs, and accuracy. We find evidence that the selection of task-relevant information occurs through the orthogonalization of relevant and irrelevant representations, demonstrating how our framework can be used to relate visual representations to behavioral outputs. Together, our work provides a probabilistic framework for both constraining neural network models of vision with behavioral data and studying how the visual system extracts representations that guide decisions.

    1. Neuroscience
    Aneri Soni, Michael J Frank
    Research Article

    How and why is working memory (WM) capacity limited? Traditional cognitive accounts focus either on limitations on the number or items that can be stored (slots models), or loss of precision with increasing load (resource models). Here, we show that a neural network model of prefrontal cortex and basal ganglia can learn to reuse the same prefrontal populations to store multiple items, leading to resource-like constraints within a slot-like system, and inducing a trade-off between quantity and precision of information. Such ‘chunking’ strategies are adapted as a function of reinforcement learning and WM task demands, mimicking human performance and normative models. Moreover, adaptive performance requires a dynamic range of dopaminergic signals to adjust striatal gating policies, providing a new interpretation of WM difficulties in patient populations such as Parkinson’s disease, ADHD, and schizophrenia. These simulations also suggest a computational rather than anatomical limit to WM capacity.