Nested neural circuits generate distinct acoustic signals during Drosophila courtship

Abstract

Animal sounds are produced by patterned vibrations of specific organs, but the neural circuits that drive these vibrations are not well defined in any animal. Here we provide a functional and synaptic map of most of the neurons in the Drosophila male ventral nerve cord (the analog of the vertebrate spinal cord) that drive complex, patterned song during courtship. Male Drosophila vibrate their wings toward females during courtship to produce two distinct song modes - pulse and sine song - with characteristic features that signal species identity and male quality. We identified song-producing neural circuits by optogenetically activating and inhibiting identified cell types in the ventral nerve cord (VNC) and by tracing their patterns of synaptic connectivity in the male VNC connectome. The core song circuit consists of at least eight cell types organized into overlapping circuits, where all neurons are required for pulse song and a subset are required for sine song. The pulse and sine circuits each include a feed-forward pathway from brain descending neurons to wing motor neurons, with extensive reciprocal and feed-back connections. We also identify specific neurons that shape the individual features of each song mode. These results reveal commonalities among diverse animals in the neural mechanisms that generate multiple motor patterns from a single set of muscles.

Transforming descending input into behavior: The organization of premotor circuits in theDrosophilaMale Adult Nerve Cord connectome

“…Here, we first broadly survey the direct and indirect connectivity of DNs to the wing MNs, and specifically focus on describing circuit connectivity and structure in relation to potential roles in flight. Wing control circuits in relation to courtship in MANC are discussed in detail in (Lillvis et al, 2023).…”

“…The breakdown of subcommunity connectivity with wing and haltere MNs is shown in Figure 10–Supplement 1A. Furthermore, community 8 and its subcommunities may be implicated in courtship-related behaviors, as many neurons that are likely positive for fruitless (identified by Lillvis et al, 2023), a transcription factor necessary for sex-specific neuronal development, are found within these communities (Figure 10–Supplement 1B).…”

“… A. Synaptic input fractions contributed by individual subcommunities to wing and haltere MNs of a group. B. Putative courtship-related communities as indicated by LM-EM matching to fruitless -positive neuron types (Lillvis et al, 2023). …”

“…IN06B066 group 16779 has connectivity with Tect INs (see Figure 12F). Identification of the TN1a, dPR1, vPR9 and vMS11 cell types in MANC by Lillvis et al, 2023. D. Lateralized wing and proximal wing campaniform sensilla sensory neuron connectivity to Tect INs and IN06B066 group 22716.…”

“…The full set of WTct/HTct DNs is shown in Figure 10A, with example morphologies of several DNs implicated in wing-related behaviors shown in Figure 10B and followed up on in the next sections. Of the WTct/HTct DNs, only a single pair of DNs (DNa08) has (Lillvis et al, 2023).…”