Paolo Ioalè

Homing Behavior of Pigeons after Telencephalic Ablations

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 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 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.

The avian hippocampus: Evidence for a role in the development of the homing pigeon navigational map

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.

The Avian Hippocampus, Homing in Pigeons and the Memory Representation of Large-Scale Space

Abstract 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.

Does pigeon homing depend on stimuli perceived during displacement

SummarySimilar experiments as described in part I (Wallraff, 1980b) were conducted in Italy. 12 releases at distances of 80–180 km showed, in most cases, similar behaviour of “cueless” transported pigeons and control pigeons, but some gradual difference in the degree of homeward directedness and, at least sometimes, in homing speed. This suggests that, in the area investigated, stimuli perceived during displacement contribute to the orientation behaviour of the birds after release. Usually, however, successful homing does not depend on these stimuli. The experiments suggest the conclusion that there is some (minor) difference in the mode of pigeon navigation in different geographic areas, probably depending on varying environmental conditions.

Unimpaired acquisition of spatial reference memory, but impaired homing performance in hippocampal-ablated pigeons

Hippocampal ablated homing pigeons have been shown to suffer a retrograde spatial reference memory deficit involving a preoperatively acquired homeward orientation response based on local cues around a previously visited release site. Here we report that the postoperative acquisition of such a response is unimpaired. Initially, 25 hippocampal ablated and 11 sham-operated controls were given 5 training releases from each of two sites. In the subsequent experimental releases from the two training sites, the controls and half the hippocampal-ablated pigeons had their navigational maps rendered dysfunctional via an anosmic procedure. Nonetheless, both groups successfully oriented homeward, indicating that the hippocampal-ablated pigeons were unimpaired in the acquisition and implementation of directionally useful information around the training sites to direct a homeward orientation response. The remaining half of the hippocampal-ablated pigeons who were not rendered anosmic, and thus served as controls, also oriented homeward. The data indicate that, for hippocampal-ablated homing pigeons, postoperative acquisition is unimpaired in the same spatial reference memory task where a robust retrograde impairment was observed. However, the hippocampal-ablated pigeons were impaired in the time required to return home, indicating a deficit in homing performance beyond the initial orientation stage.

Homing pigeons do extract directional information from olfactory stimuli

SummaryTwo groups of pigeons were kept from fledging time in two cages fully exposed to winds. From time to time, the cage containing experimentals was additionally exposed to an artificial air current coming from a specific direction and carrying a scent of benzaldehyde. When both groups were exposed to benzaldehyde scent during transportation and at the release site, the control birds flew homeward, whereas the experimentals oriented in the direction roughly opposite that from which they were used to perceiving the benzaldehyde at the loft. When benzaldehyde was not applied, experimental pigeons were homeward oriented like controls.

Pigeon Homing: Cues Detected During the Outward Journey Influence Initial Orientation

The initial orientation of homing pigeons released from the same site can be significantly different according to the odorous stimuli perceived during the outward journey. In fact, differences in orientation of pigeons transported to the same release site by different routes (“detour effect”) resulted only when the birds were allowed to perceive the odors of the areas crossed during the outward journey. Moreover, birds carried in the same vehicle were different in orientation when subjected to a different pattern of olfactory stimulation during the journey.

Navigational abilities of adult and experienced homing pigeons deprived of olfactory or trigeminally mediated magnetic information

SUMMARY Anatomical evidence and conditioning experiments have suggested that magnetoreceptors innervated by the ophthalmic branch of the trigeminal nerve are located in the upper beak of homing pigeons. Following these findings it has been proposed that the trigeminally-mediated magnetorececeptors are able to detect magnetic field intensity, which might be useful for a position finding mechanism for pigeons homing from unfamiliar locations. Recent data have shown that, in inexperienced pigeons, section of the ophthalmic branch of the trigeminal nerve does not impair navigational abilities. Similarly, no impairment was observed if the trigeminal section was performed on young pigeons, before they have had the opportunity to learn a navigational map. By contrast, section of the olfactory nerve either in adult inexperienced pigeons or in young birds before map learning, disrupted their homing performance. Nevertheless, because a magnetic map mechanism requires training flights for learning the magnetic gradient of the territory around the loft, the question remains as to whether the navigational performance of adult experienced pigeons can be affected by lack of magnetic information. To answer this question we extensively group-trained adult pigeons and then surgically deprived them of either olfactory or trigeminally mediated magnetic information, prior to testing their navigational abilities. The birds deprived of trigeminally mediated magnetic information displayed similar navigational abilities as intact control pigeons, whereas the olfactory-deprived pigeons were dramatically impaired in homing. Our data show that even in trained adult pigeons, olfactory cues are needed for homing from unfamiliar locations and that the lack of magnetic information does not affect navigational abilities of experienced adult homing pigeons.

Hippocampus and homing in pigeons: left and right hemispheric differences in navigational map learning

One‐month‐old, inexperienced homing pigeons, prior to any opportunity to learn a navigational map, were subjected to either right or left unilateral ablation of the hippocampal formation (HF). These pigeons were then held together with a group of age‐matched control birds in an outdoor aviary, where they were kept for about 3 months with the opportunity to learn a navigational map. When subsequently tested for navigational map learning at about 4 months of age posthatching, control and right HF‐ablated pigeons were equally good at orienting homeward from distant, unfamiliar locations, indicating successful navigational map learning. By contrast, left HF‐ablated pigeons were impaired in orienting homeward, indicating a failure to learn a navigational map. Interestingly, both right and left HF‐ablated pigeons displayed impaired homing performance relative to controls. These results suggest that different aspects of homing pigeon navigation may be lateralized to different hemispheres, and in particular, the HF of the different hemispheres. The left HF appears critical for navigational map learning, i.e. determining an approximate direction home from distant, unfamiliar locations. The right HF, and possibly the left HF as well, appear to play an important role in local navigation near the loft, which is likely based on familiar landmarks.

Navigational abilities of homing pigeons deprived of olfactory or trigeminally mediated magnetic information when young

SUMMARY Anatomical evidence and conditioning experiments have recently suggested that magnetoreceptors are located in the upper beak of homing pigeons, where they are innervated by the ophthalmic branch of the trigeminal nerve. These findings have raised the issue of whether the trigeminally mediated magnetoreception is involved in the navigational mechanisms of homing pigeons. Recent data have shown that, in inexperienced pigeons, section of the ophthalmic branch of the trigeminal nerve does not impair navigational abilities, whereas the navigational performance of inexperienced pigeons is disrupted after section of the olfactory nerve. Nevertheless, the issue of whether the stimuli available during development of the navigational mechanism can influence the types of cues used in determining the direction of displacement remains unresolved. To address this issue, we surgically deprived young pigeons of either olfactory or trigeminally mediated magnetic information, and then later tested their navigational abilities subsequent to an intensive training flight program of up to 10 km in different directions. The birds deprived of trigeminally mediated magnetic information when young developed navigational abilities at the same level as intact control pigeons, whereas the olfactory deprived pigeons displayed randomly scattered initial orientation and poor homing performance. Our data show that olfactory cues are needed for the development of navigational abilities from unfamiliar locations and that the lack of magnetic information does not affect the development of homing abilities.