Neural network organization for courtship-song feature detection in Drosophila

authors: Christa A. Baker, Claire McKellar, Rich Pang, Aljoscha Nern, Sven Dorkenwald, Diego A. Pacheco, Nils Eckstein, Jan Funke, Barry J. Dickson, Mala Murthy
doi: 10.1016/j.cub.2022.06.019

CITATION

Baker, C. A., McKellar, C., Pang, R., Nern, A., Dorkenwald, S., Pacheco, D. A., Eckstein, N., Funke, J., Dickson, B. J., & Murthy, M. (2022). Neural network organization for courtship-song feature detection in Drosophila. Current Biology, S0960982222009782. https://doi.org/10.1016/j.cub.2022.06.019

ABSTRACT

Animals communicate using sounds in a wide range of contexts, and auditory systems must encode behaviorally relevant acoustic features to drive appropriate reactions. How feature detection emerges along auditory pathways has been difficult to solve due to challenges in mapping the underlying circuits and characterizing responses to behaviorally relevant features. Here, we study auditory activity in the Drosophila melanogaster brain and investigate feature selectivity for the two main modes of fly courtship song, sinusoids and pulse trains. We identify 24 new cell types of the intermediate layers of the auditory pathway, and using a new connectomic resource, FlyWire, we map all synaptic connections between these cell types, in addition to connections to known early and higher-order auditory neuronsโ€”this represents the first circuit-level map of the auditory pathway. We additionally determine the sign (excitatory or inhibitory) of most synapses in this auditory connectome. We find that auditory neurons display a continuum of preferences for courtship song modes and that neurons with different song-mode preferences and response timescales are highly interconnected in a network that lacks hierarchical structure. Nonetheless, we find that the response properties of individual cell types within the connectome are predictable from their inputs. Our study thus provides new insights into the organization of auditory coding within the Drosophila brain.

fleeting notes

neurons in the AMMC show preferences to courtship song modes
the auditory connectome is highly recurrent

  • the first circuit level map of the auditory pathway including sign of most synapses

  • some AMMC auditory neurons have been characterized like B1

  • neural responses can be predicted by the responses of their inputs
    recurrent

  • focused on the WED, anterior ventrolateral protocerebrum (AVLP) and the posterior ventrolateral protocerebrum (PVLP)

  • created split lines for auditory neurons that project to the WED/VLP. Screened 1041 split lines and generated stable lines for 117 of the sparsest expression in the brain. then selected 65 for functional imaging

  • determined the preference for pulse, sine, and noise for each cell type

  • 31% of neurons were pulse preferring

  • 31 % of neurons were sine preferring

  • 38% of neurons responded to both pulse and sine (intermediate)

  • pulse preferring neurons tended to have sine preferring inhibition and vice versa

  • song mode preferences of the 28 cell types in the paper may underlie responses brain-wide

    • WED/VLP auditory neurons send projections throughout the central brain
  • pulse preferring neurons were overwhelmingly cholinergic

  • sine preferrring neurons were a mix of GABAergic and cholinergic

  • the auditory connectome features dense interconnectivity throughout the network.

    • there is some preferential connectivity within a preference category
  • cell types have extensive connectivity between cell types with different song modes

  • there is not pulse and sine song processing pathways

  • sine and pulse preference arises early in the pathway but connections between different cells creates a continuum of preferences

  • paths through the network are dominated by recurrent connections

    • there is little hierarchical organization
  • in addition to song mode preference, there is also diversity of response timescales

  • sine song neurons have longer response time constants

    • diversity of time constants may be important for processing multiple timescale song structures
  • song representations are present in 33/36 central brain areas

    • auditory circuits are highly interconnected to circuits in other modalities and functions