Nociceptive neurons respond to multimodal stimuli in Manduca sexta

Abstract

The caterpillar Manduca sexta produces a highly stereotyped strike behavior in response to noxious thermal or mechanical stimuli to the abdomen. This rapid movement is targeted to the site of the stimulus, but the identities of the nociceptive sensory neurons are currently unknown. It is also not known if both mechanical and thermal stimuli are detected by the same neurons. Here we show that the likelihood of a strike increases with the strength of the stimulus and that activity in nerves innervating the body wall increases rapidly in response to noxious stimuli. Both mechanical and thermal stimuli to the dorsal body wall activate the same sensory unit suggesting it represents a multimodal neuron. This is further supported by the effects of rapidly repeated thermal or mechanical stimuli which cause a depression of neuronal responsiveness that is generalized across modalities. Mapping the receptive fields of neurons responding to strong thermal stimuli indicate that these multimodal, nociceptive units are produced by class γ multi-dendritic neurons in the body wall.

I. The Era Beyond Eisemann et al. (1984): Insect pain in the 21st century

“…Specialized multidendritic neurons that respond tile the body walls of Drosophila melanogaster and Manduca sexta larvae. These cells exclusively respond to noxious stimuli and are anatomically similar to known vertebrate nociceptors (e.g., with dendritic branching throughout the epidermal layer; Caron et al, 2020;Grueber et al, 2001;Tracey et al, 2003; Figure 1). The noxious-stimuli-sensing function of these cells is expected to be adaptively beneficial in ecologically relevant contexts (e.g., mediating the avoidance of parasitoid wasp attacks in D. melanogaster; Hwang et al, 2007).…”

Pain and Suffering in Farmed Animals: First Steps Towards Better Understanding and Management (Musk and Clutton, 2024) - Insects

“…Class IV multidendritic neurons that respond exclusively to noxious stimuli (heat, chemical and mechanical stimuli) are found from the first instar (e.g., right after egg hatch) in larval fruit flies (Hwang et al 2007;Lopez-Bellido et al 2019); their branched dendritic morphology extending below the surface of the larval epidermis is reminiscent of vertebrate nociceptors as well (Tracey et al 2003). Tobacco hornworm moth larvae also have anatomically similar sensory cells that respond to noxious heat and mechanical stress (Grueber et al 2001;Caron et al 2020). Adult fruit fly sensory neurons with the ion channel pickpocket have been found to be responsible for mediating responses to noxious heat (Khuong et al 2019).…”