Feedback from Network States Generates Variability in a Probabilistic Olfactory Circuit

Variability is a prominent feature of behavior and is an active element of certain behavioral strategies. To understand how neuronal circuits control variability, we examined the propagation of sensory information in a chemotaxis circuit of C. elegans where discrete sensory inputs can drive a probabilistic behavioral response. Olfactory neurons respond to odor stimuli with rapid and reliable changes in activity, but downstream AIB interneurons respond with a probabilistic delay. The interneuron response to odor depends on the collective activity of multiple neurons—AIB, RIM, and AVA—when the odor stimulus arrives. Certain activity states of the network correlate with reliable responses to odor stimuli. Artificially generating these activity states by modifying neuronal activity increases the reliability of odor responses in interneurons and the reliability of the behavioral response to odor. The integration of sensory information with network states may represent a general mechanism for generating variability in behavior. [Display omitted] •Interneurons in an olfactory circuit have variable responses to a fixed odor input•Interneurons participate in collective network states that correlate with behavior•Reliability of the AIB interneuron’s odor response depends on the network activity state•Chemical synapses from the RIM interneuron increase variability of the odor response Even when a stimulus invariably activates a sensory neuron, the motor output/behavior is probabilistic because of variability in the network state of interneurons downstream of the sensory neuron. Manipulating the activity of these interneurons relative to one another can drive olfactory responses in C. elegans to be more deterministic.