Anna Gagliardo

Separate processing mechanisms for encoding of geometric and landmark information in the avian hippocampus

Domestic chicks bilaterally or unilaterally lesioned to the hippocampus were trained to search for food hidden beneath sawdust by ground‐scratching in the centre of a large enclosure, the correct position of food being indicated by a local landmark in the absence of any extra‐enclosure visual cues. At test, the landmark was removed or displaced at a distance from its original position. Results showed that sham‐operated chicks and chicks with a lesion of the left hippocampus searched in the centre, relying on large‐scale geometric information provided by the enclosure, whereas chicks with a lesion of either the right hippocampus or both hippocampi were completely disoriented (landmark removed) or searched close to the landmark shifted from the centre (landmark displaced). These results indicate that encoding of geometric features of an enclosure occurs in the right hippocampus even when local information provided by a landmark would suffice to localize the goal; encoding based on local information, in contrast, seems to occur outside the hippocampus. These findings provide evidence that the left and right avian hippocampi play different roles in spatial cognition, a phenomenon which had been documented previously only for the human hippocampus.

Testing the role of sensory systems in the migratory heading of a songbird

SUMMARY The identification of the sensory cues and mechanisms by which migratory birds are able to reach the same breeding and wintering grounds year after year has eluded biologists despite more than 50 years of intensive study. While a number of environmental cues have been proposed to play a role in the navigation of birds, arguments still persist about which cues are essential for the experience based navigation shown by adult migrants. To date, few studies have tested the sensory basis of navigational cues used during actual migration in the wild: mainly laboratory based studies or homing during the non-migratory season have been used to investigate this behaviour. Here we tested the role of olfactory and magnetic cues in the migration of the catbird (Dumetella carolinensis) by radio tracking the migration of birds with sensory manipulations during their actual migratory flights. Our data suggest that adult birds treated with zinc sulphate to produce anosmia were unable to show the same orientation as control adults, and instead reverted to a direction similar to that shown by juveniles making their first migration. The magnetic manipulation had no effect on the orientation of either adults or juveniles. These results allow us to propose that the olfactory sense may play a role in experience based migration in adult catbirds. While the olfactory sense has been shown to play a role in the homing of pigeons and other birds, this is the first time it has been implicated in migratory orientation.

Forty years of olfactory navigation in birds.

Summary Forty years ago, Papi and colleagues discovered that anosmic pigeons cannot find their way home when released at unfamiliar locations. They explained this phenomenon by developing the olfactory navigation hypothesis: pigeons at the home loft learn the odours carried by the winds in association with wind direction; once at the release site, they determine the direction of displacement on the basis of the odours perceived locally and orient homeward. In addition to the old classical experiments, new GPS tracking data and observations on the activation of the olfactory system in displaced pigeons have provided further evidence for the specific role of olfactory cues in pigeon navigation. Although it is not known which odours the birds might rely on for navigation, it has been shown that volatile organic compounds in the atmosphere are distributed as fairly stable gradients to allow environmental odour-based navigation. The investigation of the potential role of olfactory cues for navigation in wild birds is still at an early stage; however, the evidence collected so far suggests that olfactory navigation might be a widespread mechanism in avian species.

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.

Oceanic navigation in Cory's shearwaters: evidence for a crucial role of olfactory cues for homing after displacement

SUMMARY Pelagic birds, which wander in the open sea most of the year and often nest on small remote oceanic islands, are able to pinpoint their breeding colony even within an apparently featureless environment, such as the open ocean. The mechanisms underlying their surprising navigational performance are still unknown. In order to investigate the nature of the cues exploited for oceanic navigation, Corys shearwaters, Calonectris borealis, nesting in the Azores were displaced and released in open ocean at about 800 km from their colony, after being subjected to sensory manipulation. While magnetically disturbed shearwaters showed unaltered navigational performance and behaved similarly to unmanipulated control birds, the shearwaters deprived of their sense of smell were dramatically impaired in orientation and homing. Our data show that seabirds use olfactory cues not only to find their food but also to navigate over vast distances in the ocean.

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.

Homing pigeons only navigate in air with intact environmental odours : A test of the olfactory activation hypothesis with GPS data loggers

A large body of evidence has shown that anosmic pigeons are impaired in their navigation. However, the role of odours in navigation is still subject to debate. While according to the olfactory navigation hypothesis homing pigeons possess a navigational map based on the distribution of environmental odours, the olfactory activation hypothesis proposes that odour perception is only needed to activate a navigational mechanism based on cues of another nature. Here we tested experimentally whether the perception of artificial odours is sufficient to allow pigeons to navigate, as expected from the olfactory activation hypothesis. We transported three groups of pigeons in air-tight containers to release sites 53 and 61 km from home in three different olfactory conditions. The Control group received natural environmental air; both the Pure Air and the Artificial Odour groups received pure air filtered through an active charcoal filter. Only the Artificial Odour group received additional puffs of artificial odours until release. We then released pigeons while recording their tracks with 1 Hz GPS data loggers. We also followed non-homing pigeons using an aerial data readout to a Cessna plane, allowing, for the first time, the tracking of non-homing homing pigeons. Within the first hour after release, the pigeons in both the Artificial Odour and the Pure Air group (receiving no environmental odours) showed impaired navigational performances at each release site. Our data provide evidence against an activation role of odours in navigation, and document that pigeons only navigate well when they perceive environmental odours.

Migratory Navigation in Birds: New Opportunities in an Era of Fast-Developing Tracking Technology

Summary Birds have remained the dominant model for studying the mechanisms of animal navigation for decades, with much of what has been discovered coming from laboratory studies or model systems. The miniaturisation of tracking technology in recent years now promises opportunities for studying navigation during migration itself (migratory navigation) on an unprecedented scale. Even if migration tracking studies are principally being designed for other purposes, we argue that attention to salient environmental variables during the design or analysis of a study may enable a host of navigational questions to be addressed, greatly enriching the field. We explore candidate variables in the form of a series of contrasts (e.g. land vs ocean or night vs day migration), which may vary naturally between migratory species, populations or even within the life span of a migrating individual. We discuss how these contrasts might help address questions of sensory mechanisms, spatiotemporal representational strategies and adaptive variation in navigational ability. We suggest that this comparative approach may help enrich our knowledge about the natural history of migratory navigation in birds.