Neural Representation of Object Approach in a Decision-Making Motor Circuit

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Abstract
Although behavior is ultimately guided by decision-making neurons and their associated networks, the mechanisms underlying neural decision-making in a behaviorally relevant context remain mostly elusive. To address this question, we analyzed goldfish escapes in response to distinct visual looming stimuli with high-speed video and compared them with electrophysiological responses of the Mauthner cell (M-cell), the threshold detector that initiates such behaviors. These looming stimuli evoke powerful and fast body-bend (C-start) escapes with response probabilities between 0.7 and 0.91 and mean latencies ranging from 142 to 716 ms. Chronic recordings showed that these C-starts are correlated with M-cell activity. Analysis of response latency as a function of the different optical parameters characterizing the stimuli suggests response threshold is closely correlated to a dynamically scaled function of angular retinal image size, θ(t), specifically κ(t) = θ(t− δ ×e−βθ(t − δ), where the exponential term progressively reduces the weight of θ(t). Intracellular recordings show that looming stimuli typically evoked bursts of graded EPSPs with peak amplitudes up to 9 mV in the M-cell. The proposed scaling function κ(t) predicts the slope of the depolarizing envelope of these EPSPs and the timing of the largest peak. An analysis of the firing rate of presynaptic inhibitory interneurons suggests the timing of the EPSP peak is shaped by an interaction of excitatory and inhibitory inputs to the M-cell and corresponds to the temporal window in which the probabilistic decision of whether or not to escape is reached.