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

• Published in: Current biology 2017-01, Vol.27 (2), p.279-285
• Main Authors: Gaede, Andrea H., Goller, Benjamin, Lam, Jessica P.M., Wylie, Douglas R., Altshuler, Douglas L.
• Format: Article
• Language: English
• Subjects: Animals; avian vision; Flight, Animal - physiology; hummingbird; Motion Perception; Neurons - cytology; Neurons - physiology; optic flow; Photic Stimulation; pigeon; Songbirds - physiology; visual motion processing; Visual Pathways; zebra finch
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2016.11.041

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. •Neuroanatomy and visual guidance data suggest neural specialization for hovering•We recorded from neurons responding to visual direction and speed in three species•Unlike in other species, hummingbird visual nuclei are responsive to all directions•Motion processing neurons in hummingbirds prefer fast speeds Direction- and velocity-selective global motion neurons in a key visual nucleus show strong preference for forward motion in all tetrapods studied until now. Gaede et al. show that hummingbirds exhibit expansion in the direction preference domain and differences in velocity tuning, compared to other avian species.