Multisensory integration in C. elegans
Section snippets
C. elegans performs multisensory integration
All animals navigate in complex natural environments that contain both dangers and valuable sources, such as predators and food. Many of these sources are represented by more than one sensory cue. Thus, animals need to process multiple sensory cues in order to make decisions that benefit survival and reproduction. Behavioral paradigms used to investigate multisensory integration in C. elegans have been developed by taking advantage of the sensitivity of the worms to an array of sensory
Polymodal sensory neurons
Sensory neurons in C. elegans have the capability to be what is referred to as ‘polymodal’ [28]. This has been demonstrated for many of the sensory neurons using optical imaging, laser/genetic ablation and behavioral analysis, such as the ASH sensory neurons that have been shown to respond to an array of aversive stimuli of different modalities, including mechanosensation, noxious stimuli, pH, quinine, and food odors to direct sensorimotor responses [13, 19, 20, 27•, 29, 30, 31, 32, 33, 34•, 35
Functional significance of multisensory integration
Overall, we have reviewed a number of multisensory integration behaviors and possible underlying mechanisms in C. elegans (Figure 1). Together, these studies suggest that multisensory integration can take place at different layers of the nervous system using synaptic and non-synaptic communication under various contexts. Here, we propose several important functional consequences of multisensory integration. First, integrating sensory cues of multiple modalities allows animals to better extract
Conflict of interest statement
Nothing declared.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
Acknowledgments
D.D.G. was supported by a National Institute of Neurological Disease and Stroke (NINDS) National Institutes of Health (NIH) Predoctoral Fellowship (F31NS080628). Work in the laboratory of M.N.N. was supported in part by NINDS, NIH (R01NS056443, R01NS091070) and National Institute of General Medical Sciences, NIH (R01GM098931). Work in the laboratory of Y.Z. is supported in part by The National Institute on Deafness and Other Communication Disorders, NIH (R01DC009852) and National Institute of
References (89)
- et al.
A cortical circuit for gain control by behavioral state
Cell
(2014) - et al.
The multifaceted interplay between attention and multisensory integration
Trends Cogn Sci
(2010) - et al.
Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans
Neuron
(1991) - et al.
The neural circuit for touch sensitivity in Caenorhabditis elegans
J Neurosci
(1985) - et al.
C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog
Nat Neurosci
(2010) - et al.
Neural architecture of hunger-dependent multisensory decision making in C. elegans
Neuron
(2016) - et al.
HEN-1, a secretory protein with an LDL receptor motif, regulates sensory integration and learning in Caenorhabditis elegans
Cell
(2002) - et al.
Feeding status and serotonin rapidly and reversibly modulate a Caenorhabditis elegans chemosensory circuit
Proc Natl Acad Sci U S A
(2004) - et al.
In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents
EMBO J
(2005) - et al.
Neuropeptide signaling remodels chemosensory circuit composition in Caenorhabditis elegans
Nat Neurosci
(2013)
Humidity sensation requires both mechanosensory and thermosensory pathways in Caenorhabditis elegans
Proc Natl Acad Sci U S A
A G-protein alpha subunit, GOA-1, plays a role in C. elegans avoidance behavior of strongly alkaline pH
Commun Integr Biol
Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons
Neuron
Light and pheromone-sensing neurons regulates cold habituation through insulin signalling in Caenorhabditis elegans
Nat Commun
Serotonin differentially modulates Ca2+ transients and depolarization in a C. elegans nociceptor
J Neurophysiol
Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis
Nature
Dissecting the serotonergic food signal stimulating sensory-mediated aversive behavior in C. elegans
PLoS One
A pheromone influences larval development in the nematode Caenorhabditis elegans
Science
A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans
Nature
A multilevel multimodal circuit enhances action selection in Drosophila
Nature
Context-dependent modulation reconfigures interactive sensory-mediated microcircuits in Caenorhabditis elegans
Curr Opin Neurobiol
Modulation of C. elegans touch sensitivity is integrated at multiple levels
J Neurosci
A sexually conditioned switch of chemosensory behavior in C. elegans
PLoS One
Spatial attention can modulate audiovisual integration at multiple cortical and subcortical sites
Eur J Neurosci
A top-down cortical circuit for accurate sensory perception
Neuron
Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing
Science
Sensation-to-cognition cortical streams in attention-deficit/hyperactivity disorder
Hum Brain Mapp
Comparing and exploring the sensory processing patterns of higher education students with attention deficit hyperactivity disorder and autism spectrum disorder
Am J Occup Ther
Reduced modulation of thalamocortical connectivity during exposure to sensory stimuli in ASD
Autism Res
Sensorimotor difficulties are associated with the severity of autism spectrum conditions
Front Integr Neurosci
Neurophysiological hyperresponsivity to sensory input in autism spectrum disorders
J Neurodev Disord
The structure of the nervous system of the nematode Caenorhabditis elegans
Philos Trans R Soc Lond B Biol Sci
Odorant-selective genes and neurons mediate olfaction in C. elegans
Cell
A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans
PLoS Biol
Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue
Nature
Normal and mutant thermotaxis in the nematode Caenorhabditis elegans
Proc Natl Acad Sci U S A
C. elegans responds to chemical repellents by integrating sensory inputs from the head and the tail
Curr Biol
Neural regulation of thermotaxis in Caenorhabditis elegans
Nature
Experience-dependent modulation of C. elegans behavior by ambient oxygen
Curr Biol
A carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans
Proc Natl Acad Sci U S A
Food sensitizes C. elegans avoidance behaviours through acute dopamine signalling
EMBO J
Cross-modulation of homeostatic responses to temperature, oxygen and carbon dioxide in C. elegans
PLoS Genet
Neuronal substrates of complex behaviors in C. elegans
Annu Rev Neurosci
A seven-transmembrane receptor that mediates avoidance response to dihydrocaffeic acid, a water-soluble repellent in Caenorhabditis elegans
J Neurosci
Cited by (33)
Using neurons to maintain autonomy: Learning from C. elegans
2023, BioSystemsCombinational exposure to hydroxyatrazine increases neurotoxicity of polystyrene nanoparticles on Caenorhabditis elegans
2023, Science of the Total EnvironmentMaking sense of sensory behaviors in vector-borne helminths
2022, Trends in ParasitologyCitation Excerpt :While osm-9 and tax-4 have been linked to chemosensory and thermosensory transduction in filarial nematodes, the chemoreceptive GPCRs have yet to be studied experimentally [36]. Other nematode sensory modalities (e.g., thermal and mechanical) often use the same or similar components as the chemosensory pathway, allowing integration of multiple stimuli [88]. For example, GCs, which can operate downstream of chemoreceptors, can receive thermal cues directly and synthesize cGMP to activate TAX-2/TAX-4 [85,89], and TRPs can be primary mechanosensory receptors [90,91].
A single chemosensory GPCR is required for a concentration-dependent behavioral switching in C. elegans
2022, Current BiologyCitation Excerpt :Together, our results confirm that the worm does indeed employ the labeled-line theory concept to its advantage in an interesting way using two different sensory neurons expressing the same receptor. The AIB neurons—the first-layer interneurons downstream of both AWC and ASH—receive and process glutamatergic signals from AWC and ASH to mediate DMTS concentration-dependent behavioral switching (Figure 7H).11,33,38,41,71,72 The AIB neurons trigger crawling reversals in response to low levels of glutamate released from the ASH neurons responding to low levels of quinine.
Can insects feel pain? A review of the neural and behavioural evidence
2022, Advances in Insect PhysiologyCitation Excerpt :Another problem with this fruit fly study is that it does not provide evidence that satisfies this criterion's requirement for “centralised, integrative processing of information involving a common measure of value”. When both competing stimuli are experienced simultaneously, the two sensory inputs may interact via simple neural mechanisms without involving centralised integration (as demonstrated in the nematode Caenorhabditis elegans [Rhabditida: Rhabditidae]: Ghosh et al., 2016, 2017; Irvine, 2020; Shinkai et al., 2011). In a more complex study, adult fruit flies were conditioned to associate an odour with an appetitive stimulus (ethanol or sucrose).
Caenorhabditis elegans learning in a structured maze is a multisensory behavior
2021, iScienceCitation Excerpt :This is intuitively in agreement with the argument of the multisensory nature of food location in the maze. Recent work has established C. elegans’ multisensory integration (Ghosh et al., 2016, 2017) through cellular mechanisms and neuronal circuit cross-talk. We find that time passed in combination with change of environment results in loss of learning (Figure 3A).
- *
These authors contributed equally to this work.