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Abstract Once considered mere structural support cells in the nervous system, glia have recently been demonstrated to play pivotal roles in sensorimotor processing and to directly respond to sensory stimuli. However, their response properties and contributions to sensory-induced behaviors remain little understood. InCaenorhabditis elegans, the amphid sheath glia (AMsh) directly respond to aversive odorants and mechanical stimuli, but their precise transduction machinery and their behavioral relevance remain unclear. We investigated the role of AMsh in mechanosensation and their impact on escape behaviors inC. elegans. We found that nose touch stimuli in immobilized animals induced a slow calcium wave in AMsh, which coincided with the termination of escape reversal behaviors. Genetic ablation of AMsh resulted in prolonged reversal durations in response to nose touch, but not to harsh anterior touch, highlighting the specificity of AMsh’s role in distinct escape behaviors. Mechanotransduction in AMsh requires the α-tubulin MEC-12 and the ion channels ITR-1 and OSM-9, indicating a unique mechanosensory pathway that is distinct from the neighboring ASH neurons. We find that GABAergic signaling mediated by the GABA-A receptor orthologs LGC-37/8 and UNC-49 play a crucial role in modulating the duration of nose touch-induced reversals. We conclude that in addition to aversive odorant detection, AMsh mediate mechanosensation, play a pivotal role in terminating escape responses to nose touch, and provide a mechanism to maintain high sensitivity to polymodal sensory stimuli. SignificancePolymodal nociceptive sensory neurons have the challenge of multitasking across sensory modalities. They must respond to dangerous stimuli of one modality, but also adapt to repeated nonthreatening stimuli without compromising sensitivity to harmful stimuli from different modalities. Here we show that a pair of glia in the nematodeC. elegansmodulate the duration of nose-touch induced escape responses. We identify several molecules involved in the transduction of mechanical stimuli in these cells and show that they use the signaling molecule GABA to modulate neural function. We propose a mechanism through which these glia might function to maintain this polysensory neuron responsive to dangerous stimuli across different modalities.
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Stimulus-dependent learning and memory in the neotropical ant Ectatomma ruidum
ABSTRACT Learning and memory are major cognitive processes strongly tied to the life histories of animals. In ants, chemotactile information generally plays a central role in social interaction, navigation and resource exploitation. However, in hunters, visual information should take special relevance during foraging, thus leading to differential use of information from different sensory modalities. Here, we aimed to test whether a hunter, the neotropical ant Ectatomma ruidum, differentially learns stimuli acquired through multiple sensory channels. We evaluated the performance of E. ruidum workers when trained using olfactory, mechanical, chemotactile and visual stimuli under a restrained protocol of appetitive learning. Conditioning of the maxilla labium extension response enabled control of the stimuli provided. Our results show that ants learn faster and remember for longer when trained using chemotactile or visual stimuli than when trained using olfactory and mechanical stimuli separately. These results agree with the life history of E. ruidum, characterized by a high relevance of chemotactile information acquired through antennation as well as the role of vision during hunting.
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- Award ID(s):
- 1755342
- PAR ID:
- 10392963
- Date Published:
- Journal Name:
- Journal of Experimental Biology
- Volume:
- 224
- Issue:
- 9
- ISSN:
- 0022-0949
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1242/jeb.238535
