Having the nerve to home: trigeminal magnetoreceptor versus olfactory mediation of homing in pigeons.

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.

Relevance of visual cues for orientation at familiar sites by homing pigeons: an experiment in a circular arena.

Whether pigeons use visual landmarks for orientation from familiar locations has been a subject of debate. By recording the directional choices of both anosmic and control pigeons while exiting from a circular arena we were able to assess the relevance of olfactory and visual cues for orientation from familiar sites. When the birds could see the surroundings, both anosmic and control pigeons were homeward oriented. When the view of the landscape was prevented by screens that surrounded the arena, the control pigeons exited from the arena approximately in the home direction, while the anosmic pigeons' distribution was not different from random. Our data suggest that olfactory and visual cues play a critical, but interchangeable, role for orientation at familiar sites.

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.

The ontogeny of the homing pigeon navigational map: evidence for a sensitive learning period.

Homing pigeons can learn a navigational map by relying on the heterogeneous distribution of atmospheric odours in the environment. To test whether there might be a sensitive period for learning an olfactory-based navigational map, we maintained a group of young pigeons in an aviary screened from the winds until the age of three to four months post-fledging. Subsequently, the screens were removed and the pigeons were exposed to the winds and the environmental odours they carry for three months. One control group of pigeons was held in a similar aviary but exposed to the winds immediately upon Hedging, while another control group of pigeons was allowed free-flight. When the pigeons from the three groups were released from two distant release sites at about six months of age post-fledging, the two control groups were found to be equally good at orientating and returning home, while the experimental pigeons held in the shielded aviary for the first three months post-fledging were unable to orientate homeward and they were generally unsuccessful in returning home. This result supports the hypothesis that environmental experience during the first three months post-fledging is critical for some aspect of navigational map learning and that navigational map learning displays sensitive period-like properties.

Pigeon orientation: effects of the application of magnets under overcast skies.

To verify the existence of a magnetic compass in birds, researchers have often released homing pigeons under overcast skies that are equipped with bar magnets on various parts of their body. In particular, Keeton was successful in finding disorientation in overcast conditions in a first series of tests, but not in a second series. The experiments reported here attempt to explain this contradiction on the basis of findings obtained by releasing pigeons equipped in a way similar to that reported in Keeton's tests and pigeons equipped in a way similar to that reported by other authors.

Further experiments on the relationship between hippocampus and orientation following phase-shift in homing pigeons.

Following a clock- or phase-shift of the light dark cycle, hippocampal lesioned pigeons (Columba livia) consistently display a larger deviation in vanishing bearings away from the homeward direction compared to intact birds; an effect never seen in unshifted birds. In Experiment 1, control and hippocampal lesioned pigeons oriented similarly after being held 1 week under artificial lighting in the absence of a phase-shift. Housing under artificial light by itself does not result in between group orientation differences. In Experiment 2, control and hippocampal lesioned pigeons oriented equally well under overcast conditions, indicating that both groups had a functional magnetic compass. The between group difference in orientation following phase-shift does not appear to be a consequence of control birds being able to use both the sun and earth's magnetic field for orientation and the hippocampal lesioned pigeons only being able to use the sun. In Experiment 3, lengthening the time held under 6-h clock-shift from 1 to 2 weeks had no effect on the magnitude of the difference in orientation, but fast shifting produced clearer effects than slow shifting. Taken together, the data suggest that hippocampal lesions alter how a pigeon responds to a rapidly changing light-dark cycle, particularly following a fast-shift manipulation, suggesting an as yet unspecified relationship between the avian hippocampus and the circadian rhythm(s) that regulate sun compass orientation.

Hippocampal participation in navigational map learning in young homing pigeons is dependent on training experience.

The homing pigeon navigational map is perhaps one of the most striking examples of a naturally occurring spatial representation of the environment used to guide navigation. In a previous study, it was found that hippocampal lesions thoroughly disrupt the ability of young homing pigeons held in an outdoor aviary to learn a navigational map. However, since that study an accumulation of anecdotal data has hinted that hippocampal-lesioned young pigeons allowed to fly during their first summer could learn a navigational map. In the present study, young control and hippocampal-lesioned homing pigeons were either held in an outdoor aviary or allowed to fly during the time of navigational map learning. At the end of their first summer, the birds were experimentally released to test for navigational map learning. Independent of training experience, control pigeons oriented homeward during the experimental releases demonstrating that they learned a navigational map. Surprisingly, while the aviary-held hippocampal-lesioned pigeons failed to learn a navigational map as reported previously, hippocampal-lesioned birds allowed flight experience learned a navigational map indistinguishable from the two control groups. A subsequent experiment revealed that the navigational map learned by the three groups was based on atmospheric odours. The results demonstrate that hippocampal participation in navigational map learning depends on the type of experience a young bird pigeon has, and presumably, the type of navigational map learned.

Homing in pigeons: the role of the hippocampal formation in the representation of landmarks used for navigation.

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.

Pigeon homing: site simulation experiments with bird-borne direction recorders.

Previous experiments showed that pigeons allowed to smell olfactory cues at a 'false' release site, and subsequently transported to and released from another unfamiliar locality, oriented according to the home direction at the false site but eventually homed despite their wrong initial orientation. In the above 'site simulation' experiments, data collection was restricted to the initial bearings and homing performance, and no information was obtained on the actual route flown by pigeons. Route correction in site simulation tests is now investigated by releasing pigeons equipped with bird-borne direction recorders to track their route. Our results show that the experimental birds can actually fly for a long time in wrong directions, related to the home direction at the false release site, before correcting their path to the true homeward direction. This correction occurs 2 h or more after release, when the birds are supposed to have recovered from the anaesthesia of their olfactory membranes which they had been subjected to just prior to release. This result confirms the basic role of the olfactory information, collected during the outward journey, in the pigeon's homing process.

The homing pigeon hippocampus and the development of landmark navigation.

The role of the homing pigeon hippocampal formation was examined in the development of loft fidelity and landmark navigation. During the course of five summers, different groups of young pigeons (hippocampal-lesioned, control-lesioned, and unoperated controls) were given free flight experience followed by short distance training and experimental releases. In Experiment 1, a census of which loft each pigeon entered revealed that hippocampal lesioned pigeons displayed less loft fidelity than controls. In Experiment 2 and 3, the percent of young birds lost during their first summer of training and their first experimental release was examined. Despite displaying similarly good homeward-oriented vanishing bearings, significantly more hippocampal lesioned pigeons were lost compared to control groups. The results support the hypothesis that the homing pigeon hippocampal formation participates in the learning/operation of a spatial representation of local landmarks near the loft that can be used for loft recognition and navigation.

The neuroethology of cognitive maps: contributions from research on the hippocampus and homing pigeon navigation.

The rich ethological tradition that characterizes the homing behavior of pigeons offers an excellent opportunity to examine the importance of the hippocampal formation for the regulation of spatial cognitive mechanisms. The present review summarizes both anatomical and behavioral data obtained in researches on the pigeon hippocampal formation that have been performed over the last 12 years. Pathway connection studies and investigations on the neurochemical organization of the avian hippocampal formation show that this structure shares many similarities with the mammalian hippocampus and provide the basis for structural as well as functional homology. The initial research on the role of the hippocampal formation in the homing behavior showed that this brain structure is likely to be involved in phenomena of spatial cognition. Therefore, the homing behavior of pigeons has been extensively used as an experimental model to investigate the role of the hippocampal formation in spatial cognition related to a naturally occurring behavior. These studies have revealed that the hippocampal formation plays a fundamental role in the learning of a navigational map based on atmospheric odors, but it doesn't seem to be involved in the operation of such a map. In contrast, both the learning and the operation of a navigational map based on the recognition of familiar landmarks require a functional hippocampal formation. Further investigations indicated that these functions of the hippocampal formation are mediated by its involvement in the use of the sun compass, and suggested that the hippocampal formation plays a fundamental role in a cognitive process in which the sun compass is specifically used to learn about the location of stimuli in space. The studies reviewed in the present paper have provided a considerable amount of experimental data both on the anatomical/neurochemical organization of the avian hippocampal formation and on the role played by this brain structure in spatial cognition. The future development of these researches will need to consider the contribution to hippocampal function of specific transmitter systems that are involved in hippocampal circuitry. In particular, the afferent cholinergic system and some of the peptidergic systems intrinsic to the hippocampal formation deserve particular attention in view of their possible involvement in the acquisition and/or operation of spatial cognitive abilities by homing pigeons.

Pigeon homing: The influence of topographical features in successive releases at the same site.

A new device, the direction-recorder, offered the possibility to extend earlier studies of homing behaviour of pigeons when relevant topographical elements (mountains and large tracts of water) interpose between the release site and the home loft. Three series of experiments were carried out at three different sites to investigate intraindividual and interindividual variability in subsequent tosses from the same locality. Two release sites were chosen behind a mountain chain with respect to home; at the third site homeward directed route crosses the sea. From our results it turns out that homing pigeons may adopt different strategies. Moreover, a wide intraindividual variability was observed in repeated tosses at the same site; some pigeons remained faithful to the first route, whereas other birds tried successive new routes which, in most cases, were significantly shorter than previous ones. This result indicates that pigeons try, and are actually able, to improve their performance in subsequent releases from the same site.

Hippocampal participation in the sun compass orientation of phase-shifted homing pigeons.

The orientation of phase-shifted control and hippocampal lesioned homing pigeons with previous homing experience was examined to investigate the possible participation of the hippocampal formation in sun compass orientation. Hippocampal lesioned pigeons displayed appropriate shifts in orientation indicating that such birds possess a functional sun compass that is used for orientation. However, their shift in orientation was consistently larger than in control pigeons revealing a difference in orientation never observed in pigeons that have not undergone a phase shift. Although alternative interpretations exist, the data suggest the intriguing possibility that following a change in the light-dark cycle, the hippocampal formation participates in the re-entrainment of a circadian rhythm that regulates sun compass orientation.

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.

Olfactory bulb size, odor discrimination and magnetic insensitivity in hummingbirds.

Relative olfactory bulb size with respect to telencephalic hemispheres (olfactory ratio) was measured in five species of hummingbirds. Trochiliformes were found to be next to last among 25 avian orders with respect to olfactory bulb development. One hummingbird species, the White-vented Violetear (Colibri serrirostris), was trained in a successive go/no-go discrimination task, and learned to feed or not to feed from a container dependent on the olfactory stimuli associated with it. Test birds learned to discriminate amyl acetate vs. turpentine essence, jasmine essence vs. lavender essence, eucalyptus essence vs. no odor, beta-ionone vs. no odor, carvone vs. eucalyptol. In contrast, 1-phenylethanol vs. beta-ionone discrimination, two odorants which appear similar to humans, was unsuccessful. Using a similar procedure, attempts were made to condition a White-vented Violetear and a Versicolored Emerald (Amazilia versicolor) to magnetic stimuli. The birds were unable to discriminate between a normal field and an oscillating field (square wave, 1 Hz, amplitude +/- 0.40 G).

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.

Impaired retention of preoperatively acquired spatial reference memory in homing pigeons following hippocampal ablation.

Hippocampal-parahippocampal-ablated homing pigeons have been shown to suffer a retrograde loss of information used in the recognition of their home loft. Here we report that the range of retrograde deficits includes spatial reference memory in the form of information gained from repeated training sites that can be used to direct a homeward orientation response. Following 8 training releases from each of two sites, 28 of 42 homing pigeons underwent hippocampal-parahippocampal ablation. In the subsequent test releases from the two sites, untreated controls whose navigational map was rendered temporarily dysfunctional by an anosmic procedure showed no impairment in determining the home direction, indicating the successful retention and utilization of directionally useful information around the release sites. Hippocampal-ablated controls who were not rendered anosmic and thus had access to their navigational map also showed no impairment in determining the home direction, indicating no general impairment in initial orientation as a result of hippocampal ablation. In contrast, hippocampal-ablated pigeons whose navigational map was rendered temporarily dysfunctional failed to successfully orient homeward from the training sites, indicating impairment in the retention and/or implementation of directional information gathered at the release sites during training. The data reveal a spatial reference memory deficit involving pre-ablation acquired directional information in homing pigeons following hippocampal ablation.

Dorsomedial forebrain ablations and home loft association behavior in homing pigeons.

In a series of experiments which involved only short distance experimental releases (800 m or less and within view of the home loft), it was demonstrated that dorsomedial forebrain ablated pigeons generally failed to reassociate with their home loft if the postablation experimental release took place soon postablation or if during the time between ablation and experimental release they were kept away from their home loft. In contrast, if dorsomedial forebrain ablated pigeons were allowed to recover at their home loft prior to experimental release, they succeeded in associating with their home loft in a manner similar to controls. However, only postablation exposure to a pigeon's own loft was sufficient to permit continued home loft association. Pigeons from one loft failed to associate with a foreign postablation recovery loft when released within sight of it. The results show that dorsomedial forebrain ablations result in pigeons which no longer succeed in associating with their home loft; recovery from failed home loft association behavior is possible with postablation exposure to the home loft, and a pigeon's previous association with a loft was a precondition if postablation association was to be affected. The results suggest that dorsomedial forebrain ablated pigeons retain something like a 'home loft trace' which they can use to mediate retrieval and reformation of the recognition properties needed for proper home loft association.

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.