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.

Olfactory lateralization in homing pigeons: a GPS study on birds released with unilateral olfactory inputs.

A large body of evidence has shown that pigeons rely on an olfactory-based navigational map when homing from unfamiliar locations. Previous studies on pigeons released with one nostril occluded highlighted an asymmetry in favour of the right nostril, particularly concerning the initial orientation performance of naïve birds. Nevertheless, all pigeons experiencing only unilateral olfactory input showed impaired homing, regardless of the side of the occluded nostril. So far this phenomenon has been documented only by observing the birds' vanishing bearings. In the present work we recorded the flight tracks of pigeons with previous homing experience equipped with a GPS data logger and released from an unfamiliar location with the right or the left nostril occluded. The analysis of the tracks revealed that the flight path of the birds with the right nostril occluded was more tortuous than that of unmanipulated controls. Moreover, the pigeons smelling with the left nostril interrupted their journey significantly more frequently and displayed more exploratory activity than the control birds, e.g. during flights around a stopover site. These data suggest a more important involvement of the right olfactory system in processing the olfactory information needed for the operation of the navigational map.

Navigation-induced ZENK expression in the olfactory system of pigeons (Columba livia).

A large body of evidence indicates that pigeons use olfactory cues to navigate over unfamiliar areas with a differential contribution of the left and right hemispheres. In particular, the right nostril/olfactory bulb (OB) and left piriform cortex (Cpi) have been demonstrated to be crucially involved in navigation. In this study we analysed behaviour-induced activation of the olfactory system, indicated by the expression of the immediate early gene ZENK, under different homing conditions. One experimental group was released from an unfamiliar site, the second group was transported to the unfamiliar site and back to the loft, and the third group was released in front of the loft. To evaluate the differential contribution of the left and/or right olfactory input, the nostrils of the pigeons were either occluded unilaterally or not. Released pigeons revealed the highest ZENK cell density in the OB and Cpi, indicating that the olfactory system is activated during navigation from an unfamiliar site. The groups with no plug showed the highest ZENK cell density, supporting the activation of the olfactory system probably being due to sensory input. Moreover, both Cpis seem to contribute differently to the navigation process. Only occlusion of the right OB resulted in a decreased ZENK cell expression in the Cpi, whereas occlusion of the left nostril had no effect. This is the first study to reveal neuronal activation patterns in the olfactory system during homing. Our data show that lateralized processing of olfactory cues is indeed involved in navigation over unfamiliar areas.

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

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.

Olfactory navigation in homing pigeons: the last challenge.

The olfactory navigation hypothesis of pigeon homing was recently challenged by the discovery in the upper beak of putative magnetoreceptors innervated by the ophthalmic branch of the trigeminal nerve. To assess whether the nature of the cues used for navigation is determined by the kind of stimuli to which the birds are preferentially exposed during development, we tested the navigational performance of pigeons subjected when young to section of either the ophthalmic branch of the trigeminal nerve (V1) or the olfactory nerve and then subjected to training flights after the surgery. Section of V1 had no effect on homing performance, but olfactory cues are needed for development of the navigational map.

Hippocampal-dependent familiar area map supports corrective re-orientation following navigational error during pigeon homing: a GPS-tracking study.

It is hypothesized that a central role of the vertebrate hippocampal formation (HF) in behavior is the learning and operation of a map-like representation of familiar landmarks and landscape features. One critical property of a map is that it should enable an individual to re-orient towards a goal location following a navigational error. To test this prediction on a spatial scale consistent with their naturally occurring behavior, control and HF-lesioned homing pigeons were trained from two locations and then subsequently released, while carrying portable GPS-tracking devices, following a phase-shift treatment. Analyses revealed that the HF-lesioned pigeons were less successful than control pigeons in re-orienting homewards following the phase-shift-induced error in their initial orientation. Furthermore, the observation that HF-lesioned pigeons were found to routinely ignore a land-sea landscape boundary when returning home from one of the release sites suggests that coarse landscape features may be an underappreciated source of navigational information for homing pigeons. The data demonstrate that, on a scale of tens of kilometers, homing pigeons are able to learn a hippocampal-dependent, map-like representation of familiar landmarks/landscape features that can support corrective re-orientation following a navigational error.

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

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.

Olfactory lateralization in homing pigeons: initial orientation of birds receiving a unilateral olfactory input.

It has been shown that homing pigeons (Columba livia) rely on olfactory cues to navigate from unfamiliar locations. In fact, the integrity of the olfactory system, from the olfactory mucosa to the piriform cortex, is required for pigeons to navigate over unfamiliar areas. Recently it has been shown that there is a functional asymmetry in the piriform cortex, with the left piriform cortex more involved in the use of the olfactory navigational map than the right piriform cortex. To investigate further the lateralization of the olfactory system in relation to navigational processes in carrier pigeons, we compared their homing performance after either their left or the right nostril was plugged. Contrary to our expectations, we observed an impairment in the initial orientation of the pigeons with their right nostril plugged. However, both groups released with one nostril plugged tended to be poorer than control pigeons in their homing performance. The observed asymmetry in favour of the right nostril might be due to projections from the olfactory bulbs to the contralateral globus pallidum, a structure involved in motor responses.

Finding home: the final step of the pigeons' homing process studied with a GPS data logger.

Experiments have shown that homing pigeons are able to develop navigational abilities even if reared and kept confined in an aviary, provided that they are exposed to natural winds. These and other experiments performed on inexperienced birds have shown that previous homing experiences are not necessary to determine the direction of displacement. While the cues used in the map process for orienting at the release site have been extensively investigated, the final step of the homing process has received little attention by researchers. Although there is general agreement on the relevance of visual cues in navigation within the home area, there is a lack of clear evidence. In order to investigate the final step of the homing process, we released pigeons raised under confined conditions and others that had been allowed to fly freely around the loft and compared their flight paths recorded with a Global-Positioning-System logger. Our data show that a limited view of the home area impairs the pigeons' ability to relocate the loft at their first homing flight, suggesting that the final step of the homing process is mediated via recognition of familiar visual landmarks in the home area.

Functional asymmetry of left and right avian piriform cortex in homing pigeons' navigation.

It has been shown that homing pigeons rely on olfactory cues to navigate over unfamiliar areas and that any kind of olfactory impairment produces a dramatic reduction of navigational performance from unfamiliar sites. The avian piriform cortex is the main projection field of olfactory bulbs and it is supposed to process olfactory information; not surprisingly bilateral lesions to this telencephalic region disrupt homing pigeon navigation. In the present study, we attempted to assess whether the left and right piriform cortex are differentially involved in the use of the olfactory navigational map. Therefore, we released from unfamiliar locations pigeons subjected, when adult, to unilateral ablation of the piriform cortex. After being released, the pigeons lesioned to the right piriform cortex orientated similarly to the intact controls. On the contrary, the left lesioned birds were significantly more scattered than controls, showing a crucial role of the left piriform cortex in processing the olfactory cues needed for determining the direction of displacement. However, both lesioned groups were significantly slower than controls in flying back to the home loft, showing that the integrity of both sides of the piriform cortex is necessary to accomplish the whole homing process.

Factors reducing the expected deflection in initial orientation in clock-shifted homing pigeons.

To orient from familiar sites, homing pigeons can rely on both an olfactory map and visual familiar landmarks. The latter can in principle be used in two different ways: either within a topographical map exploited for piloting or in a so-called mosaic map associated with a compass bearing. One way to investigate the matter is to put the compass and the topographical information in conflict by releasing clock-shifted pigeons from familiar locations. Although the compass orientation is in general dominant over a piloting strategy, a stronger or weaker tendency to correct towards the home direction by clock-shifted pigeons released from very familiar sites has often been observed. To investigate which factors are involved in the reduction of the deviation due to clock-shift, we performed a series of releases with intact and anosmic pigeons from familiar sites in unshifted and clock-shifted conditions and a series of releases from the same sites with naive clock-shifted birds. Our data suggest that the following factors have a role in reducing deviation due to the clock-shift: familiarity with the release site, the lack of olfactory information and some unknown site-dependent features.

The avian hippocampus, homing in pigeons and the memory representation of large-scale space.

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.

Hippocampal lesions do not disrupt navigational map retention in homing pigeons under conditions when map acquisition is hippocampal dependent.

In contrast to map-like navigation by familiar landmarks, understanding the relationship between the avian hippocampal formation (HF) and the homing pigeon navigational map has remained a challenge. With the goal of filling an empirical gap, we performed an experiment in which young homing pigeons learned a navigational map while being held in an outdoor aviary, and then half the birds were subjected to HF ablation. The question was whether HF lesion would impair retention of a navigational map learned under conditions known to require participation of HF. The pigeons, which had never flown from the aviary before, together with an additional control group that learned a navigational map with free-flight experience, were then released from two distant release sites. Contrary to expectation, the HF-lesioned birds oriented in a homeward direction in manner indistinguishable from the intact control pigeons raised in the same outdoor aviary. HF lesion did not result in a navigational map retention deficit. Together with previous results, it is now clear that regardless of the learning environment present during acquisition, HF plays no necessary role in the subsequent retention or operation of the homing pigeon navigational map.

Effects of monocular viewing on orientation in an arena at the release site and homing performance in pigeons.

Orientation and homing performance of pigeons with the left or right eye occluded were assessed in an arena at the release site and during the subsequent homing flight. Three release sites near Pisa, Italy, were used. Compared to binocular controls, monocular birds showed a bias in orientation towards the side of the viewing eye. In the arena, this bias was considerable and the mean deviation corresponded to the angle of the optical axis, suggesting a systematic error in visual representation during directional orientation. During flight after leaving the arena the directional bias decreased and the homeward orientation increased. While there was a slight lateralization of overall homing performance in favour of the right eye, there was no lateralization in directional orientation in the arena or at vanishing. Our results show that navigational mechanisms in either brain hemisphere profit from information obtained before take off and while flying over the release site. The existence and degree of lateralization is discussed in comparison to other studies that investigated homing under monocular viewing conditions.

Bilateral participation of the hippocampus in familiar landmark navigation by homing pigeons.

Recent findings indicate a different role of the left and right hippocampal formation (RHF) in homing pigeon navigational map learning. However, it remains uncertain whether the left or the RHF may play a more important role in navigation based on familiar landmarks. In the present study, we attempted to answer this question by experimentally releasing control and left and right hippocampal ablated pigeons from familiar training sites under anosmia, to render their navigational map dysfunctional, and after a phase-shift of the light-dark cycle, to place into conflict a pilotage-like landmark navigational strategy and a site-specific compass orientation landmark navigational strategy. Both left and right hippocampal ablated birds succeeded in learning to navigate by familiar landmarks, and both preferentially relied on sun-compass based, site-specific compass orientation to home. Like bilateral hippocampal lesioned birds, and in contrast to intact controls, neither ablation group adopted a pilotage-like strategy. We conclude that both the left and RHF are necessary if pilotage-like, familiar landmark navigation is to be learned or preferentially used for navigation.

Participation of the homing pigeon thalamofugal visual pathway in sun-compass associative learning.

The ascending thalamofugal visual pathway in pigeons (Columba livia) terminates in the telencephalic wulst. Characterizing the role of this pathway in visually guided behaviour has remained a challenge. To determine whether this pathway, and in particular the wulst, may participate in sun-compass-guided behaviour in homing pigeons, intact, ectostriatum-lesioned or wulst-lesioned pigeons were trained to use their sun compass to locate the direction of a food reward in an outdoor, octagonal arena. Control and ectostriatum-lesioned pigeons learned the task well, and orientated appropriately during the first trial of the last three training sessions and after a phase-shift manipulation. In contrast, the wulst-lesioned pigeons learned the task but they took more sessions to learn, and their directional choices were more scattered during the first trial of the last three training sessions and after the phase-shift manipulation. A subsequent regression analysis indicated that deeper layers of the wulst might have made more of a contribution to the observed behavioural impairments. The data indicate that the homing pigeon wulst participates in visually guided behaviour when the sun compass is used to learn the directional location of a goal.