Population dynamics of the thalamic head direction system during drift and reorientation

The head direction (HD) system is classically modeled as a ring attractor network1,2 which ensures a stable representation of the animal’s head direction. This unidimensional description popularized the view of the HD system as the brain’s internal compass3,4. However, unlike a globally consistent magnetic compass, the orientation of the HD system is dynamic, depends on local cues and exhibits remapping across familiar environments5. Such a system requires mechanisms to remember and align to familiar landmarks, which may not be well described within the classic 1-dimensional framework. To search for these mechanisms, we performed large population recordings of mouse thalamic HD cells using calcium imaging, during controlled manipulations of a visual landmark in a familiar environment. First, we find that realignment of the system was associated with a continuous rotation of the HD network representation. The speed and angular distance of this rotation was predicted by a 2nd dimension to the ring attractor which we refer to as network gain, i.e. the instantaneous population firing rate. Moreover, the 360-degree azimuthal profile of network gain, during darkness, maintained a ‘memory trace’ of a previously displayed visual landmark. In a 2nd experiment, brief presentations of a rotated landmark revealed an attraction of the network back to its initial orientation, suggesting a time-dependent mechanism underlying the formation of these network gain memory traces. Finally, in a 3rd experiment, continuous rotation of a visual landmark induced a similar rotation of the HD representation which persisted following removal of the landmark, demonstrating that HD network orientation is subject to experience-dependent recalibration. Together, these results provide new mechanistic insights into how the neural compass flexibly adapts to environmental cues to maintain a reliable representation of the head direction.

Learning walks in an Australian desert ant, Melophorus bagoti

The Central Australian ant Melophorus bagoti is the most thermophilic ant in Australia and forages solitarily in the summer months during the hottest period of the day. For successful navigation, desert ants of many species are known to integrate a path and learn landmark cues around the nest. Ants perform a series of exploratory walks around the nest before their first foraging trip, during which they are presumed to learn about their landmark panorama. Here, we studied 15 naïve M. bagoti ants transitioning from indoor work to foraging outside the nest. In three to four consecutive days, they performed 3 to 7 exploratory walks before heading off to forage. Naïve ants increased the area of exploration around the nest and the duration of trips over successive learning walks. In their first foraging walk, the majority of the ants followed a direction explored on their last learning walk. During learning walks, the ants stopped and performed stereotypical orientation behaviours called pirouettes. They performed complete body rotations with stopping phases as well as small circular walks without stops known as voltes. After just one learning walk, these desert ants could head in the home direction from locations 2 m from the nest, although not from locations 4 m from the nest. These results suggest gradual learning of the visual landmark panorama around the foragers’ nest. Our observations show that M. bagoti exhibit similar characteristics in their learning walks as other desert ants of the genera Ocymyrmex and Cataglyphis.

Young frigatebirds learn how to compensate for wind drift

Compensating for wind drift can improve goalward flight efficiency in animal taxa, especially among those that rely on thermal soaring to travel large distances. Little is known, however, about how animals acquire this ability. The great frigatebird ( Fregata minor ) exemplifies the challenges of wind drift compensation because it lives a highly pelagic lifestyle, travelling very long distances over the open ocean but without the ability to land on water. Using GPS tracks from fledgling frigatebirds, we followed young frigatebirds from the moment of fledging to investigate whether wind drift compensation was learnt and, if so, what sensory inputs underpinned it. We found that the effect of wind drift reduced significantly with both experience and access to visual landmark cues. Further, we found that the effect of experience on wind drift compensation was more pronounced when birds were out of sight of land. Our results suggest that improvement in wind drift compensation is not solely the product of either physical maturation or general improvements in flight control. Instead, we believe it is likely that they reflect how frigatebirds learn to process sensory information so as to reduce wind drift and maintain a constant course during goalward movement.

Visual landmarks calibrate auditory space across eye movements

Visual objects that are present both before and after eye movements can act as landmarks, aiding localization of other visual stimuli. We investigated whether visual landmarks would also influence auditory localization – despite participants’ head position remaining unchanged. Participants made eye-movements from central fixation to a peripheral visual landmark, which either remained stationary or was covertly displaced. Following the movement, participants judged whether a stimulus (auditory or visual) was shifted in location relative to before the movement. Visual localization estimates shifted along with the landmark, although the landmark displacement itself went unnoticed. Interestingly, auditory localization estimates were also displaced. Thus, despite identical auditory input reaching the ears, two auditory stimuli originating from the same position were perceived as spatially distinct when the visual landmark moved. These results are consistent with the idea that auditory spatial information is encoded within an eye-centered reference frame and subject to spatial recalibration by visual landmarks.HighlightsVisual landmarks affect stimulus localization across eye movementsWe show this also for auditory stimuli, even when the head remains stableDue to a visual landmark displacement, identical auditory stimuli are perceived as shiftedThis suggests that auditory space is calibrated on eye-centered maps across saccades