Structural, Functional, and Molecular Remodeling of an Adaptive Sensorimotor Circuit

When animals are reared in different environments, the brain adapts their sensorimotor behaviors to local condi- tions. Understanding how the brain creates adaptive behavior requires dissecting how specific mechanisms for synaptic and cellular plasticity spread to system-wide modulation of sensorimotor circuits and behavior. We will develop the mating behavior of the C. elegans male as a comprehensively accessible paradigm for experience- dependent plasticity throughout a sensorimotor circuit. The C. elegans male uses a separate circuit in its tail – ~100 sensory neurons, interneurons, and motor neurons – to drive mating behavior. How this circuit executes information-processing and decision-making depends on the physical environment. When reared on flat surfaces, the male adapts his mating ritual to two-dimensions. During ‘parallel mating’, he limits his sensorimotor decision-making to sliding movements alongside his partner’s body from contact to copulation. When reared in liquids, the swimming male uses ‘spiral mating’, where sensorimotor decision-making includes three-dimensional movements like wrapping around his partner and using exploratory tail movements. Whether the sensorimotor circuit encodes parallel or spiral mating depends on life experience. Males reared in liquid are proficient at spiral mating. Males reared on plates are proficient at parallel mating. We seek synaptic, cellular, and wiring mechanisms that lead to different sensorimotor outcomes when an animal is reared in different environments. We will map the wiring diagram of the mating circuit as it adapt to 2D and 3D mating behaviors. We will record circuit-wide neural activity during parallel and spiral mating. We will use spatial transcriptomics and genetic manipulations to dissect how synaptic and cellular mechanisms lead to circuit and behavioral remodeling. We will build computational models that use neurophysiological, neuroanatomical, and neurogenetic datasets to interrelate synaptic, circuit, and behavioral mechanisms. Project Number: 1R01NS148475-01 | Fiscal Year: 2026 | NIH Institute/Center: National Institute of Neurological Disorders and Stroke (NINDS) | Principal Investigator: ARAVINTHAN SAMUEL (+1 co-PI) | Institution: HARVARD UNIVERSITY, CAMBRIDGE, MA | Award Amount: $636,084 | Activity Code: R01 | Study Section: Sensory-Motor Neuroscience Study Section[SMN] View on NIH RePORTER: https://reporter.nih.gov/project-details/11344406