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

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.

Comparative analysis of vestibular ecomorphology in birds

“…Alternatively, evolutionary changes in visual acuity, changes in the visual environment through which a bird flies, changes in how that environment is perceived, and changes in how the optical sensory afferents are processed by the brain (Gaede et al. ) might be equally as important as labyrinth morphology for maintaining adequate head stabilisation reflexes. For example, Wylie & Frost () demonstrated that the spatial planes of the optokinetic system of birds are organised with respect to the eye muscles rather than the semicircular canals.…”

“…This recently has been shown to be potentially unique in vertebrates in that it has rapid sensitivity to relative changes in global scene features in all directions (Gaede et al. ; this region in other tetrapods is more sensitive to front‐to‐back motion of the global visual field). This highlights the potential importance of global visual motion for control of balance in flight, and indicates that evolutionary adaptation of the optokinetic response may be of critical importance in the evolution of tetrapod locomotion.…”

Pretectal projections to the oculomotor cerebellum in hummingbirds (Calypte anna), zebra finches (Taeniopygia guttata), and pigeons (Columba livia)

“…In nearly all tetrapods studied to date, the typical pattern observed is that LM neurons prefer temporo‐nasal (back‐to‐front) motion across the retina, and nBOR neurons prefer naso‐temporal (front‐to‐back), upward or downward motion (Fite, ; Hoffmann & Schoppmann, ; Ibbotson, Mark, & Maddess, ; Mckenna & Wallman, ; Mustari & Fuchs, ; Winterson & Brauth, ; Wylie & Crowder, ). However, in hummingbirds, a different pattern of response properties in the LM emerged (Gaede, Goller, Lam, Wylie, & Altshuler, ). The majority of LM neurons do not prefer temporo‐nasal motion; instead, there is a more uniform distribution of preferred directions, with cells preferring upward, downward, and naso‐temporal motion as frequently as temporo‐nasal motion (Gaede et al, ).…”

“…However, in hummingbirds, a different pattern of response properties in the LM emerged (Gaede, Goller, Lam, Wylie, & Altshuler, ). The majority of LM neurons do not prefer temporo‐nasal motion; instead, there is a more uniform distribution of preferred directions, with cells preferring upward, downward, and naso‐temporal motion as frequently as temporo‐nasal motion (Gaede et al, ). Consistent with other tetrapods, there is a strong population‐level preference for temporo‐nasal motion among LM neurons of zebra finches and pigeons.…”

“…Consistent with other tetrapods, there is a strong population‐level preference for temporo‐nasal motion among LM neurons of zebra finches and pigeons. Furthermore, hummingbird and zebra finch LM neurons prefer higher velocities of visual motion than pigeon LM neurons (Gaede et al, ). This suggests a role for the LM in responding to high‐speed visual motion during hovering and collision avoidance in hummingbirds.…”