Due to technical limitations, prior studies in C. elegans have not typically considered distributed coding principles observed in other nervous systems. Instead, identified neurons have been described as dedicated encoders of specific sensory inputs or motor outputs in a context of separable, linear and mostly feed-forward sensory-to-motor pathways. This viewpoint is hard to reconcile with the largely horizontal and recurrent character of the neuronal wiring diagram. Moreover, the circuit elements in these studies overlap, suggesting that processing of various sensory modalities and computation of behavior may be performed by a common system. Here, using a single-cell resolution, brain-wide Ca2+-imaging approach developed by our group, we find that neural population dynamics exhibit a widely shared, low-dimensional component with a cyclical state space trajectory, indicative of a continuous attractor manifold. Next, by calcium imaging in free-moving worms, we find that the activities of key neurons correlate to both high level motor state as well as analog movement parameters such as speed, and that these activities map onto the state space trajectory in a well-ordered manner: trajectory bundles can be mapped to motor command states and decisions between alternate behaviors are readily observable at bundle branch points. Moreover, an analog parameter like speed drive is discernible by the position on the manifold. We argue that this dynamical organization assembles action sequences of discrete motor states and at the same time encodes graded metrics of motor intent. This study establishes, for the first time in any animal, a real-time mapping between neural and behavioral dynamics on a single-trial basis. Using chemical genetics, we find that network dynamics persist when decoupled from output by pre-motor interneuron inhibition. Moreover, manifold topology is robust and provides a framework for a sensory input, which modulates the probability of branch traversal, to produce stimulus-evoked behavioral transitions. Both results indicate that population state structure is stably maintained by intrinsic dynamics. This work shows that many neuron classes participate in a pervasive low-dimensional signal which holds the high-level motor command sequence. In mammals, cortical population dynamics produce functionality in a distributed manner; e.g. in macaque motor cortex, goal parameters are encoded across the neural population and movement is produced by collective dynamics. The character and function of the collective neural dynamics we observe suggests that despite profoundly differing neuroanatomy, the principles of C. elegans and mammalian brain function are far more similar than previously suspected.
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