A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans

Top Cited Papers
Open Access
Publisher Website
Google Scholar
Abstract
The nematode Caenorhabditis elegans, with a neuronal circuit consisting of just 302 neurons, can lay claim to being the simplest animal with a social brain. 'Social' strains of C. elegans elect to aggregate when there are bacteria to be eaten, but solitary strains do not. A new study now identifies the RMG inter/motor neuron pair as the hub for the neuronal computations involved in the integration of multiple sensory cues and making the decision to socialize. The RMG neurons are at the centre of a hub-and-spoke circuit, linking to neighbouring sensory neurons through nonsynaptic 'gap junctions'. The circuit controls the way in which neurons respond to pheromone gradients. Nematodes socialize during feeding on bacteria; this behaviour depends on sophisticated integration of multiple sensory cues by a subset of the animal's 302 neurons. The RMG neurons are identified as the hub for such computations. Non-synaptic communication through 'gap junctions' is the key to RMG's regulation of neighbouring sensory neurons such as ASK (which responds to pheromones, a functional architecture that could be generalized to several other neuronal circuits). Innate social behaviours emerge from neuronal circuits that interpret sensory information on the basis of an individual’s own genotype, sex and experience. The regulated aggregation behaviour of the nematode Caenorhabditis elegans, a simple animal with only 302 neurons, is an attractive system to analyse these circuits. Wild social strains of C. elegans aggregate in the presence of specific sensory cues, but solitary strains do not1,2,3,4. Here we identify the RMG inter/motor neuron as the hub of a regulated circuit that controls aggregation and related behaviours. RMG is the central site of action of the neuropeptide receptor gene npr-1, which distinguishes solitary strains (high npr-1 activity) from wild social strains (low npr-1 activity); high RMG activity is essential for all aspects of social behaviour. Anatomical gap junctions connect RMG to several classes of sensory neurons known to promote aggregation, and to ASK sensory neurons, which are implicated in male attraction to hermaphrodite pheromones5. We find that ASK neurons respond directly to pheromones, and that high RMG activity enhances ASK responses in social strains, causing hermaphrodite attraction to pheromones at concentrations that repel solitary hermaphrodites. The coordination of social behaviours by RMG suggests an anatomical hub-and-spoke model for sensory integration in aggregation, and points to functions for related circuit motifs in the C. elegans wiring diagram.