The Role of Motion Extrapolation in Amphibian Prey Capture

• Published in: The Journal of neuroscience 2015-11, Vol.35 (46), p.15430-15441
• Main Authors: Borghuis, Bart G, Leonardo, Anthony
• Format: Article
• Language: English
• Subjects: Animals; Caudata; Head Movements; Motion Perception - physiology; Photic Stimulation; Predatory Behavior - physiology; Psychomotor Performance - physiology; Reaction Time - physiology; Tongue - physiology; Urodela - physiology
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.3189-15.2015

Sensorimotor delays decouple behaviors from the events that drive them. The brain compensates for these delays with predictive mechanisms, but the efficacy and timescale over which these mechanisms operate remain poorly understood. Here, we assess how prediction is used to compensate for prey movement that occurs during visuomotor processing. We obtained high-speed video records of freely moving, tongue-projecting salamanders catching walking prey, emulating natural foraging conditions. We found that tongue projections were preceded by a rapid head turn lasting ∼ 130 ms. This motor lag, combined with the ∼ 100 ms phototransduction delay at photopic light levels, gave a ∼ 230 ms visuomotor response delay during which prey typically moved approximately one body length. Tongue projections, however, did not significantly lag prey position but were highly accurate instead. Angular errors in tongue projection accuracy were consistent with a linear extrapolation model that predicted prey position at the time of tongue contact using the average prey motion during a ∼ 175 ms period one visual latency before the head movement. The model explained successful strikes where the tongue hit the fly, and unsuccessful strikes where the fly turned and the tongue hit a phantom location consistent with the fly's earlier trajectory. The model parameters, obtained from the data, agree with the temporal integration and latency of retinal responses proposed to contribute to motion extrapolation. These results show that the salamander predicts future prey position and that prediction significantly improves prey capture success over a broad range of prey speeds and light levels. Neural processing delays cause actions to lag behind the events that elicit them. To cope with these delays, the brain predicts what will happen in the future. While neural circuits in the retina and beyond have been suggested to participate in such predictions, few behaviors have been explored sufficiently to constrain circuit function. Here we show that salamanders aim their tongues by using extrapolation to estimate future prey position, thereby compensating for internal delays from both visual and motor processing. Predictions made just before a prey turn resulted in the tongue being projected to a position consistent with the prey's pre-turn trajectory. These results define the computations and operating regimen for neural circuits that predict target motion.