Head-mounted sensors reveal visual attention of free-flying homing pigeons

Abstract

Gaze behavior offers valuable insights into attention and cognition. However, technological limitations have prevented the examination of animals' gaze behavior in natural, information-rich contexts; for example, during navigation through complex environments. Therefore, we developed a lightweight custom-made logger equipped with an inertial measurement unit (IMU) and GPS to simultaneously track the head movements and flight trajectories of free-flying homing pigeons. Pigeons have a limited range of eye movement, and their eye moves in coordination with their head in a saccadic manner (similar to primate eye saccades). This allows head movement to act as a proxy for visual scanning behavior. Our IMU sensor recorded the 3D movement of the birds' heads in high resolution, allowing us to reliably detect distinct saccade signals. The birds moved their head far more than necessary for maneuvering flight, suggesting that they actively scanned the environment. This movement was predominantly horizontal (yaw) and sideways (roll), allowing them to scan the environment with their lateral visual field. They decreased their head movement when they flew solo over prominent landmarks (major roads and a railway line) and also when they flew in pairs (especially when flying side by side, with the partner maintained in their lateral visual field). Thus, a decrease in head movement indicates a change in birds' focus of attention. We conclude that pigeons use their head gaze in a task-related manner and that tracking flying birds' head movement is a promising method for examining their visual attention during natural tasks.

How lovebirds maneuver through lateral gusts with minimal visual information

“…6G). These findings suggest future movement ecological studies may find value in tracking both the body and head motion of birds [as recently pioneered in a pigeon navigation study (47)] to interpret atmospheric wind orientation in birds (SI Appendix, Fig. SF36).…”

An “orientation sphere” visualization for examining animal head movements

“…Importantly though, simple examination of head orientation using the O‐sphere will tend to have greater lability and translation of points across the O‐sphere due to the signal being a composite of the head and the body (cf. Figures 3 and 4—but see stabilization of the head in birds (Frost, 2009) and Kano et al, 2018). In addition, moving animals normally have particular reason to inspect the environment more thoroughly than stationary ones (which may mean more short‐term fixations and higher transition rates).…”

“…However, the increasing use of head‐ and eye‐tracking technology in captivity using head‐mounted equipment (e.g., Williams, Mills, & Guo, 2011) means that developments in technology should now enable us to examine the head movements of wild animals. Indeed, despite reservations that such systems are likely to be suitable for wild animals moving uninhibited in their natural environment (Duchowski, 2017), Kano, Walker, Sasaki, and Biro (2018) have already demonstrated the use of a head‐tracking system on free‐flying homing pigeons, while Kane and Zamani (2014) used head‐mounted cameras to investigate how trained falcons hunt prey using visual motion cues. It therefore seems clear that similar systems will be used on wild animals soon (Kano, 2019).…”

“…Williams et al, 2011). The sophistication of such methods is, however, particularly challenging for wild animals, so simpler systems based on head, rather than eye, orientation (Wilson, Holton, et al, 2015; Wilson, Norman, et al, 2015) have proven useful on captive, but free‐flying, birds (Kane & Zamani, 2014; Kano et al, 2018). Indeed, these systems have revealed important details about how homing pigeons allocate their attention to the environment.…”

“…Specifically, the data are made up of head heading (or azimuth) in one plane and head pitch (also called elevation or dip angle) in another, perpendicular to this. Head roll (bank angle) is a third plane, although it generally changes gaze orientation minimally and is less likely to be more important than heading and pitch in environmental framing (but see Kano et al, 2018). We propose that these metrics can be conveniently examined in a single spherical visualization that we term the “orientation sphere” (O‐sphere) (cf.…”