Neurons Responsive to Global Visual Motion Have Unique Tuning Properties in Hummingbirds

Gaede, A H and Goller, B and Lam, J P M and Wylie, D R and Altshuler, D L (2017) Neurons Responsive to Global Visual Motion Have Unique Tuning Properties in Hummingbirds. Current Biology, 26 (2). pp. 279-285. ISSN 09609822

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Official URL: https://doi.org/10.1016/j.cub.2016.11.041

Abstract

Neurons in animal visual systems that respond to global optic flow exhibit selectivity for motion direction and/or velocity. The avian lentiformis mesencephali (LM), known in mammals as the nucleus of the optic tract (NOT), is a key nucleus for global motion processing [1–4]. In all animals tested, it has been found that the majority of LM and NOT neurons are tuned to temporo-nasal (back-to-front) motion [4–11]. Moreover, the monocular gain of the optokinetic response is higher in this direction, compared to naso-temporal (front-to-back) motion [12, 13]. Hummingbirds are sensitive to small visual perturbations while hovering, and they drift to compensate for optic flow in all directions [14]. Interestingly, the LM, but not other visual nuclei, is hypertrophied in hummingbirds relative to other birds [15], which suggests enhanced perception of global visual motion. Using extracellular recording techniques, we found that there is a uniform distribution of preferred directions in the LM in Anna’s hummingbirds, whereas zebra finch and pigeon LM populations, as in other tetrapods, show a strong bias toward temporo-nasal motion. Furthermore, LM and NOT neurons are generally classified as tuned to ‘‘fast’’ or ‘‘slow’’ motion [10, 16, 17], and we predicted that most neurons would be tuned to slow visual motion as an adaptation for slow hovering. However, we found the opposite result: most hummingbird LM neurons are tuned to fast pattern velocities, compared to zebra finches and pigeons. Collectively, these results suggest a role in rapid responses during hovering, as well as in velocity control and collision avoidance during forward flight of hummingbirds.

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