Investigation of cue dependent feeding behaviour in Caenorhabditis elegans reveals a critical mechanosensory dependent microcircuit in the control of pharyngeal pumping

Abstract

Both external and internal sensory cues are critical for modulating feeding behaviour. C. elegans provides a powerful model to study feeding behaviour, since one can reduce a multimodal cue to its component parts to show how different modalities impact the execution of simple behaviours. On food, worms pump at high levels but display a dramatic reduction in pumping rate in the absence of food. The main aims of the studies reported herein were twofold, 1) to examine behavioural plasticity in feeding behaviour in C. elegans and 2), again in in C. elegans, to determine which sensory modalities regulate feeding behaviour.

Plasticity in feeding behaviour was studied by examining innate and acquired behavioural responses of C. elegans to olfactory cues in on- and off-food contexts (Chapters 3-4). Alcohols affected chemotaxis in a dose-dependent manner but reduced pharyngeal pumping in the presence and absence of food. These results were followed up by investigating plasticity of chemotaxis and pharyngeal pumping to butan-1-ol and butanone. Only pre-exposing worms to pairing of butanone and food enhanced chemotaxis to butanone in subsequent tests, without altering pharyngeal pumping to butanone. These findings indicate that a specific component of the olfactory modality regulates chemotaxis and is subject to plasticity.

The modalities that regulate feeding behaviour of C. elegans were investigated by behavioural analysis which revealed elevated pharyngeal pumping to a mechanosensory cue presented in the form of microspheres (beads). These beads selectively stimulated pumping if they were small enough to be ingested by the worms. Therefore, the physical contact and an enteric response are critical to drive pumping rate (Chapter 5). However, these mechanosensory cues that drive pharyngeal pumping failed to evidence plasticity in the pharynx as a consequence of a novel pairing between paradigm-based on olfactory and mechanosensory cues (Chapter 7).

Genetic studies revealed that serotonin and dopamine were critical determinants in the mechanical stimulation of pumping (Chapter 6). Despite having normal feeding behaviour on food, dop-4 (tm1392) mutants failed to respond to beads. Further mutant analysis revealed that the pharyngeal neurones, I2, were critical in the bead-induced pumping rate, since ablation of I2 neurones occluded the response to beads. A novel assay that scored the change in pump rate as worms entered food indicated that dopamine released outside the pharynx acted via DOP-4 receptors, expressed in I2 neurones, to accelerate the rate at which worms reached maximal pump rate on food. This evidenced a previously undiscovered dopaminergic volume transmission in the control of food-induced pharyngeal pumping and provides a distinct contribution to multiple mechanisms that allow the rapid increase in pumping as the worm transits from and off- to an on-food environment. These observations highlight a role for dopamine in the anticipation of nutrition provided by the ingestion of a potential food source in the worm.

More information

Identifiers

ORCID for Lindy Holden-Dye: orcid.org/0000-0002-9704-1217

ORCID for Vincent O'connor: orcid.org/0000-0003-3185-5709

ORCID for Steven Glautier: orcid.org/0000-0001-8852-3268

Catalogue record

Export record