Multisensory Integration in Caenorhabditis elegans in Comparison to Mammals

Abstract

Multisensory integration refers to sensory inputs from different sensory modalities being processed simultaneously to produce a unitary output. Surrounded by stimuli from multiple modalities, animals utilize multisensory integration to form a coherent and robust representation of the complex environment. Even though multisensory integration is fundamentally essential for animal life, our understanding of the underlying mechanisms, especially at the molecular, synaptic and circuit levels, remains poorly understood. The study of sensory perception in Caenorhabditis elegans has begun to fill this gap. We have gained a considerable amount of insight into the general principles of sensory neurobiology owing to C. elegans’ highly sensitive perceptions, relatively simple nervous system, ample genetic tools and completely mapped neural connectome. Many interesting paradigms of multisensory integration have been characterized in C. elegans, for which input convergence occurs at the sensory neuron or the interneuron level. In this narrative review, we describe some representative cases of multisensory integration in C. elegans, summarize the underlying mechanisms and compare them with those in mammalian systems. Despite the differences, we believe C. elegans is able to provide unique insights into how processing and integrating multisensory inputs can generate flexible and adaptive behaviors. With the emergence of whole brain imaging, the ability of C. elegans to monitor nearly the entire nervous system may be crucial for understanding the function of the brain as a whole.

Sensory integration of food availability and population density during the diapause exit decision involves insulin-like signaling inCaenorhabditis elegans

“…Accordingly, C. elegans employs multiple polymodal sensory neurons that express multiple GPCRs to detect different stimuli (Troemel et al, 1995), such as ASH which can detect a variety of noxious stimuli, AWA which responds to numerous chemoattractants (Bargmann, 2006; Ferkey et al, 2021), and AWC which responds to both odors and temperature (Biron et al, 2008; Kuhara et al, 2008). While vertebrates and insects do utilize polymodal neurons, most notably in nociception (Boivin et al, 2023; Emery et al, 2016; Emery and Wood, 2019), sensory integration in such organisms is typically performed via a multilayer model in which modality-specific neurons converge onto higher order brain regions (Ghosh et al, 2017; Yu et al, 2022), a key example being the “one neuron – one receptor” principle observed in mammals and flies wherein each olfactory neuron classes usually only express one olfactory receptor, and signals from each become integrated in further regions of the olfactory bulb (Serizawa et al, 2004; Task et al, 2022). Our results help us better understand how a single neuron performs complex computations of multiple sensory inputs and underscores how the computational power of nematode nervous systems (all about 300 neurons) is vastly underestimated by cell number alone.…”

Intricate response dynamics enhances stimulus discrimination in the resource-limitedC. eleganschemosensory system

“…Invertebrates, particularly those with small nervous systems, have shallower networks with limited neural layers. As such, chemosensory information is likely to be integrated, even partially, already at the level of the sensory layer (Bargmann 2006; Sengupta 2007; Ferkey, Sengupta, and L’Etoile 2021; Ghosh et al 2017; Yu, Xue, and Chen 2022; Metaxakis, Petratou, and Tavernarakis 2018). But how can such sensory systems with limited sensory resources uniquely encode many different stimuli?…”