Neurexin controls plasticity of a mature, sexually dimorphic neuron

• Published in: Nature (London) 2018-01, Vol.553 (7687), p.165-170
• Main Authors: Hart, Michael P., Hobert, Oliver
• Format: Article
• Language: English
• Subjects: 14/19; 631/378/2583; 631/378/87; Animal reproduction; Animals; Axonogenesis; Axons; Brain; Caenorhabditis elegans; Caenorhabditis elegans - cytology; Caenorhabditis elegans - physiology; Caenorhabditis elegans Proteins - metabolism; Cell Adhesion Molecules, Neuronal - metabolism; Dendrites; Developmental plasticity; GABAergic Neurons - cytology; GABAergic Neurons - metabolism; gamma-Aminobutyric Acid - metabolism; Hermaphroditic Organisms - physiology; Humanities and Social Sciences; Male; Males; Mating behavior; Morphology; multidisciplinary; Nematodes; Nerve proteins; Neural circuitry; Neurites - metabolism; Neuronal Plasticity - physiology; Neurons; Neuroplasticity; Physiological aspects; Science; Sex; Sex Characteristics; Sexual Behavior, Animal - physiology; Sexual dimorphism; Structure-function relationships; Synapses - metabolism; Synaptic plasticity; γ-Aminobutyric acid
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature25192

During development and adulthood, brain plasticity is evident at several levels, from synaptic structure and function to the outgrowth of dendrites and axons. Whether and how sex impinges on neuronal plasticity is poorly understood. Here we show that the sex-shared GABA ( γ -aminobutyric acid)-releasing DVB neuron in Caenorhabditis elegans displays experience-dependent and sexually dimorphic morphological plasticity, characterized by the stochastic and dynamic addition of multiple neurites in adult males. These added neurites enable synaptic rewiring of the DVB neuron and instruct a functional switch of the neuron that directly modifies a step of male mating behaviour. Both DVB neuron function and male mating behaviour can be altered by experience and by manipulation of postsynaptic activity. The outgrowth of DVB neurites is promoted by presynaptic neurexin and antagonized by postsynaptic neuroligin, revealing a non-conventional activity and mode of interaction of these conserved, human-disease-relevant factors. The DVB neuron in Caenorhabditis elegans shows male-specific morphological plasticity that is controlled by neurexin and influences mating behaviour. Rewiring an invertebrate neuron Learning and memory are universal processes in the animal kingdom, but structural plasticity in invertebrate nervous systems has been hard to demonstrate. Michael Hart and Oliver Hobert describe extensive, experience-dependent synaptic rewiring of the DVB neuron—which controls mating behaviour in Caenorhabditis elegans —in adult male worms. They also show that neurexin and neuroligin have a role in the rewiring process. This is a new function for these cell adhesion molecules, which have been associated with human neurological and mental health disorders.