When given repeated training from a location, homing pigeons acquire the ability to use familiar landmarks to navigate home. Both control and hippocampal-lesioned pigeons succeed in learning to use familiar landmarks for homing. However, the landmark representations that guide navigation are strikingly different. Control and hippocampal-lesioned pigeons were initially given repeated training flights from two locations. On subsequent test days from the two training locations, all pigeons were rendered anosmic to eliminate use of their navigational map and were phase- or clock-shifted to examine the extent to which their learned landmark representations were dependent on the use of the sun as a compass. We show that control pigeons acquire a landmark representation that allows them to directly use landmarks without reference to the sun to guide their flight home, called "pilotage". Hippocampal-lesioned birds only learn to use familiar landmarks at the training location to recall the compass direction home, based on the sun, flown during training, called "site-specific compass orientation." The results demonstrate that for navigation of 20 km or more in a natural field setting, the hippocampal formation is necessary if homing pigeons are to learn a spatial representation based on numerous independent landmark elements that can be used to directly guide their return home.
In a first experiment, dorsomedial forebrain ablated birds showed similar homeward orientation when compared to untreated controls independent of whether the birds were released from a previous training site or a site they had never been before. However, although all control birds returned to the home loft, only 2 of 28 birds with lesions homed successfully. In a subsequent experiment, both sham operated control birds and birds with lesions of the visual Wulst homed successfully when released only 800 m from and in full view of their respective home lofts. Pigeons with dorsomedial forebrain lesions, however, failed to return to their respective home lofts. The results show that (1) the avian dorsomedial forebrain plays a critical role in that step of the homing process by which a pigeon returns to its home loft once in its vicinity, and that (2) the failure to reassociate with the home loft is a likely result of deficient recognition of the home loft and/or its surrounding area. In an additional experiment, pigeons with Wulst lesions were shown to orient as controls and to successfully return to the home loft when released from two distant sites. This experiment demonstrated that the avian Wulst plays no necessary role in the homing behavior of pigeons.
SUMMARY The ability of pigeons to find their way home from unfamiliar sites located up to hundreds of kilometers away is well known, but the mechanisms underlying this ability remain controversial. One proposed mechanism is based on the suggestion that pigeons are equipped with magnetoreceptors that can enable the detection of either the earth's magnetic field and/or magnetic field anomalies in the local terrain over which the pigeons fly. Recent reports have suggested that these magnetoreceptors are located in the upper beak where they are innervated by the ophthalmic branch of the trigeminal nerve. Moreover, this nerve has been shown to mediate pigeons' ability to discriminate the presence versus the absence of a magnetic field anomaly in a conditioning situation. In the present study, however, we show that an intact ophthalmic branch of the trigeminal nerve is neither necessary nor sufficient for good homing performance from unfamiliar locations, but that an intact olfactory nerve is necessary.
The extraordinary navigational ability of homing pigeons provides a unique spatial cognitive system to investigate how the brain is able to represent past experiences as memory. In this paper, we first summarize a large body of lesion data in an attempt to characterize the role of the avian hippocampal formation (HF) in homing. What emerges from this analysis is the critical importance of HF for the learning of map-like, spatial representations of environmental stimuli used for navigation. We then explore some interesting properties of the homing pigeon HF, using for discussion the notion that the homing pigeon HF likely displays some anatomical or physiological specialization(s), compared to the laboratory rat, that account for its participation in homing and the representation of large-scale, environmental space. Discussed are the internal connectivity among HF subdivisions, the occurrence of neurogenesis, the presence of rhythmic theta activity and the electrophysiological profile of HF neurons. Comparing the characteristics of the homing pigeon HF with the hippocampus of the laboratory rat, two opposing perspectives can be supported. On the one hand, one could emphasize the subtle differences in the properties of the homing pigeon HF as possible departure points for exploring how the homing pigeon HF may be adapted for homing and the representation of large-scale space. Alternatively, one could emphasize the similarities with the rat hippocampus and suggest that, if homing pigeons represent space in a way different from rats, then the neural specializations that would account for the difference must lie outside HF. Only future research will determine which of these two perspectives offers a better approximation of the truth.
Young homing pigeons were subjected to hippocampal lesion before being placed in their permanent loft to examine what effect such treatment may have on the development of their navigational map, which supports homing from distant unfamiliar locations. When later released from 3 distant unfamiliar locations, the hippocampal-lesioned pigeons were impaired in taking up a homeward bearing. The results identify a deficit in the acquisition of navigational ability after hippocampal ablation in homing pigeons. The results strongly suggest a deficit in navigational map acquisition, but alternative interpretations cannot be excluded. The findings offer the first insight into the central neural structures involved in the acquisition of the pigeon navigational map. Further, the results identify the hippocampus as a structure critical for the regulation of navigational behavior that manifests itself in a natural setting.
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