Cross-modal modulation gates nociceptive inputs in Drosophila

Curr Biol. 2023 Apr 10;33(7):1372-1380.e4. doi: 10.1016/j.cub.2023.02.032. Epub 2023 Mar 8.

Abstract

Animals' response to a stimulus in one sensory modality is usually influenced by other modalities.1 One important type of multisensory integration is the cross-modal modulation, in which one sensory modality modulates (typically inhibits) another. Identification of the mechanisms underlying cross-modal modulations is crucial for understanding how sensory inputs shape animals' perception and for understanding sensory processing disorders.2,3,4 However, the synaptic and circuit mechanisms that underlie cross-modal modulation are poorly understood. This is due to the difficulty of separating cross-modal modulation from multisensory integrations in neurons that receive excitatory inputs from two or more sensory modalities5-in which case it is unclear what the modulating or modulated modality is. In this study, we report a unique system for studying cross-modal modulation by taking advantage of the genetic resources in Drosophila. We show that gentle mechanical stimuli inhibit nociceptive responses in Drosophila larvae. Low-threshold mechanosensory neurons inhibit a key second-order neuron in the nociceptive pathway through metabotropic GABA receptors on nociceptor synaptic terminals. Strikingly, this cross-modal inhibition is only effective when nociceptor inputs are weak, thus serving as a gating mechanism for filtering out weak nociceptive inputs. Our findings unveil a novel cross-modal gating mechanism for sensory pathways.

Keywords: Drosophila; GABAergic modulation; cross-modal modulation; multisensory integration; nociceptive behavior; presynaptic inhibition; sensory gating.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Afferent Pathways
  • Animals
  • Drosophila*
  • Neurons / physiology
  • Nociception*
  • Nociceptors