Landscape heterogeneity and novelty drive avian oscillatory flight behaviour during forebrain Wulst-dependent visual map learning

Homing pigeons rely on familiar landscape features in learning a visual map, which is orchestrated by the forebrain visual Wulst and hippocampus. Recent global positioning system tracking studies showed that pigeons with damage to the visual Wulst or hippocampus exhibited a still poorly understood, persistent oscillatory flight behaviour, unlike intact pigeons whose oscillations decrease with experience. To evaluate whether landscape heterogeneity influences the extent of these oscillations, we compared the flight behaviour of both intact and Wulst-lesioned pigeons when flying over the sea versus land. Regardless of treatment, pigeons exhibited less oscillatory flight behaviour over the homogeneous landscape of the sea. Further releases from familiar and unfamiliar sites tested whether oscillatory flight behaviour may be influenced by the level of familiarity with the landscape. Indeed, intact pigeons reduced their oscillatory behaviour as landscape familiarity increased. In contrast, Wulst-damaged pigeons persisted in displaying robust oscillatory flight behaviour regardless of the level of landscape familiarity, suggesting that previously experienced landscapes remained relatively unfamiliar to them. The data support the hypothesis that oscillatory flight behaviour reflects active visual scanning, most pronounced over novel, heterogeneous landscapes, contributing to visual map learning. Further, the data suggest a crucial role of the forebrain Wulst for such learning.