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

Andrea H Gaede,Benjamin Goller,Jessica P.M Lam,Douglas R Wylie,Douglas L Altshuler

doi:10.1016/j.cub.2016.11.041

Andrea H Gaede, Benjamin Goller + Show 3 more

Open Access

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

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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 aretuned 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.

Highlights

We first identified the preferred direction of lentiformis mesencephali (LM) neurons by presenting visual motion in each of eight directions, 45 apart
The current study demonstrates that hummingbird LM neurons deviate strongly from the tetrapod pattern by having no directional bias at the population level (Figure 2)
Other previous studies, which used random dot-fields in pigeons, classified 82% of measured LM cells as ‘‘fast’’ (>6/s) and 18% as ‘‘slow’’ (

Summary

Introduction

We first identified the preferred direction of LM neurons by presenting visual motion in each of eight directions, 45 apart. Each motion stimulus lasted 5 s and was bounded by 5 s pauses. Raw extracellular recordings are shown for one hummingbird cell during a full trial (Figure 1A) and two zebra finch cells during a portion of a trial, with higher temporal resolution (Figure 1D). Single units were isolated offline using amplitude or template spike sorting (Figures 1E, 1F, and S1B; see Supplemental Experimental Procedures)

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