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Visual signals of self-motion in the pretectum of a flying zebra finch Press, Eric Richard

Abstract

Many animals including birds and humans depend on global visual motion, commonly termed optic flow, to guide movement through natural environments. In all tetrapods, the pretectal nucleus lentiformis mesencephali (LM, which is homologous to the mammalian pretectal nucleus of the optic tract) contains retina-recipient neurons that respond to optic flow stimuli and demonstrate tuning with respect to direction, speed, and in the spatiotemporal domain. Neural inactivation experiments and electrophysiology paired with eye tracking demonstrate that LM is implicated in image stabilizing eye movements such as the optokinetic response. Given the physiology and connectivity of LM, it is expected to also play a role in the analysis of optic flow during locomotion and other gaze stabilizing behaviours such as the optomotor responses. However, LM function has never been investigated in unrestrained, behaving animals. The motivating hypothesis for this research is that the activity of LM neurons is modulated by optic flow during natural locomotion. Because subcortical optic flow pathways to the cerebellum are well-defined in birds and thought to serve an important role in flight, zebra finches and their flight behaviours were investigated. Extracellular electrophysiology paired with high-throughput motion tracking was developed to record spiking activity of LM neurons in freely flying zebra finches. Analyses compare the responses of LM neurons to flight-induced optic flow and exogenous large-field motion stimuli presented to head-fixed subjects. Most neurons responded during flight in accordance with their tuning properties determined during head- fixation. Neurons that preferred forward motion were typically inhibited by flight-induced backward motion, but some could be excited by exogenous forward motion, suggesting a portion of LM neurons faithfully report visually driven signals during flight. Neurons that responded to exogenous optic flow in the frontal visual field were highly active during flight, suggesting they may respond to flight-induced visual expansion. These findings suggest LM participates in visuomotor transformations during locomotion, extending its role beyond oculomotor behaviours.

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Attribution-NonCommercial-NoDerivatives 4.0 International