Routing the Flow of Sensory Signals Using Plastic Responses to Bursts and Isolated Spikes: Experiment and Theory

Abstract

Processing complex sensory environments efficiently requires a diverse array of neural coding strategies. Neural codes relying on specific temporal patterning of action potentials may offer advantages over using solely spike rate codes. In particular, stimulus-dependent burst firing may carry additional information that isolated spikes do not. We use the well characterized electrosensory system of weakly electric fish to address how stimulus-dependent burst firing can determine the flow of information in feedforward neural circuits with different forms of short-term synaptic plasticity. Pyramidal cells in the electrosensory lateral line lobe burst in response to low-frequency, local (prey) signals. We show that the ability of pyramidal cells to code for local signals in the presence of additional high-frequency, global (communication) stimuli is uncompromised, while burst firing is reduced. We developed a bursting neuron model to understand how these effects, in particular noise-induced burst suppression, arise from interplay between incoming sensory signals and intrinsic neuronal dynamics. Finally, we examined how postsynaptic target populations preferentially respond to one of the two sensory mixtures (local vs local plus global) depending on whether the populations are in receipt of facilitating or depressing synapses. This form of feedforward neural architecture may allow for efficient information flow in the same neural pathway via either isolated or burst spikes, where the mechanisms by which stimuli are encoded are adaptable and sensitive to a diverse array of stimulus and contextual mixtures.