Anosmia impairs homing orientation but not foraging behaviour in free-ranging shearwaters.

Shearwaters deprived of their olfactory sense before being displaced to distant sites have impaired homing ability but it is unknown what the role of olfaction is when birds navigate freely without their sense of smell. Furthermore, treatments used to induce anosmia and to disrupt magneto-reception in displacement experiments might influence non-specific factors not directly related to navigation and, as a consequence, the results of displacement experiments can have multiple interpretations. To address this, we GPS-tracked the free-ranging foraging trips of incubating Scopoli's shearwaters within the Mediterranean Sea. As in previous experiments, shearwaters were either made anosmic with 4% zinc sulphate solution, magnetically impaired by attachment of a strong neodymium magnet or were controls. We found that birds from all three treatments embarked on foraging trips, had indistinguishable at-sea schedules of behaviour and returned to the colony having gained mass. However, we found that in the pelagic return stage of their foraging trips, anosmic birds were not oriented towards the colony though coastal navigation was unaffected. These results support the case for zinc sulphate having a specific effect on the navigational ability of shearwaters and thus the view that seabirds consult an olfactory map to guide them across seascapes.

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

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.

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.

Pretreatment with intravenous ketamine reduces propofol injection pain.

BACKGROUND: Paediatric procedural sedation using propofol has been shown to be safe and effective and is widely used. Pain at the injection site is a frequent complaint and can be particularly distressing for children, especially for those undergoing repeated procedures. Ketamine has analgesic properties and can diminish the incidence of propofol infusion pain in adults. The aim of the study was to investigate whether pretreatment with ketamine would reduce infusion line pain in propofol sedation in children. METHODS: We performed a prospective, randomized, double-blind trial in a paediatric sedation unit of a tertiary referral teaching hospital. A total of 122 children admitted for gastroscopy were randomly allocated into two groups. Group 1 received atropine and ketamine before propofol infusion. Group 2 received atropine, normal saline solution, and a mixture of propofol with lidocaine. The main outcome measure evaluated was pain associated with the infusion and secondary outcome measures were mean medium arterial pressure decrease and desaturation. RESULTS: The incidence of pain of the infusion was significantly lower in patients pretreated with ketamine (8% vs 37%, P = 0.0001). CONCLUSIONS: Pretreatment with ketamine (0.5 mg.kg-1) is very effective in preventing propofol infusion pain.

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.

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.

Homeward orientation of pigeons confined in a circular arena.

To investigate the ability of homing pigeons to determine the home direction at the release site before take off, we recorded the oriented movement of 17 birds at the point at which they left a circular arena. We subsequently observed the pigeons' vanishing bearings. The comparison between the orientation of each bird while leaving the arena and at its vanishing point showed that pigeons are generally able to orient in a direction close to the home direction before taking-off. This finding illustrates the possibility of studying pigeon orientation in a controllable space with evident advantages for experimentation.

Homing pigeons use olfactory cues for navigation in england

Although the use of olfactory cues in pigeon navigation is well established, the generality of olfactory navigation remains uncertain because of apparent variability in results gained by different researchers in different regions. We report the results of the first experiments investigating the effect of anosmia on homing pigeons reared in a previously uninvestigated region, southern England. In series 1, experienced birds showed little effect of anosmia induced with zinc sulphate at unfamiliar sites 30 km and 39 km from the loft, but treated birds were significantly poorer than controls at homing from an unfamiliar site 66 km distant (and in pooled results). In series 2, naive (untrained) birds, both control and zinc-sulphate-treated, showed poor homing abilities and initial orientation from sites 25 km, 36 km and 39 km from the loft. Nevertheless, in pooled results, controls showed significantly better homeward orientation than anosmic birds and were significantly more likely to home on the day of release. The most likely explanation for our results is that pigeons are able to use olfactory navigation in southern England, but that for some reason the olfactory map is relatively weak.

Piriform cortex ablations block navigational map learning in homing pigeons.

Young homing pigeons were subjected to ablations of the piriform cortex or left intact and allowed to learn a navigational map. Three months later, control and piriform cortex lesioned pigeons were released from three unfamiliar locations. Control pigeons oriented homeward indicating successful navigational map learning. In contrast, piriform cortex ablated pigeons consistently oriented east, took more time to return home and were more likely to get lost. The results demonstrate that piriform cortex ablations in young homing pigeons disrupt navigational learning. The data support the conclusion that participation of the piriform cortex is necessary for navigational map learning, and its role in navigational learning cannot be substituted for by other telencephalic olfactory processing regions. Further, the results show that the role of olfactory cues in building up the navigational map cannot be replaced by other non olfactory environmental stimuli.

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.

Memory of radial maze behavior in pigeons after ablations of the presumed equivalent of mammalian prefrontal cortex.

Pigeons were trained and postoperatively tested in an 8-arm radial maze in which 1 arm was always used for start, 3 were never baited, and 4 were always baited. Of 2 groups of pigeons, 1 (n = 6) received ablations of the postero-dorso-lateral neostriatum (PDLNS) as well as the corticoid, and the other (n = 8) was sham operated. After the surgery, in the PDLNS group the number of reference memory errors (entering the never-baited arms) was significantly increased, but the number of working memory errors (entering previously visited baited arms) was not. Two of 6 pigeons with PDLNS ablations did not show any impairment, 3 were impaired in the reference memory, and 1 was impaired in working memory. This outcome resembles behavioral effects obtained in rats with prefrontal lesions. In pigeons and rats, the lesion seems to "release" the normal "win-shift" tendency and/or impair the ability to choose correctly in simultaneous multiple-choice situations.

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.

Behavioural effects of ablations of the presumed 'prefrontal cortex' or the corticoid in pigeons.

This study further explored functional similarities of mammalian prefrontal cortex and its presumed equivalent in pigeons. Our results show that the performance of delayed alternation of pigeons in an Y-maze is impaired following ablations of the prefrontal equivalent together with the corticoid but not of the corticoid alone. In the same maze, discrimination between vertical and horizontal stripes was unimpaired regardless of the lesion. Our results added the following new information. (1) Corticoid is not essentially involved in mediation of delayed responding. (2) Like monkeys, pigeons take much fewer trials to learn delayed alternation in a maze than in an operant chamber. (3) Lesions of the pigeon equivalent of the prefrontal cortex impair delayed responding also in the new apparatus. (4) These lesions do not impair visual pattern discrimination. Our results do not contradict the hypothesis that the postero-dorso-lateral neostriatum in pigeons is comparable to the prefrontal cortex in mammals.

Homing experiments on pigeons subjected to bilateral destruction of the paratympanic organ

The paratympanic organ (PO) in birds is a specialised sensory organ whose function is still unknown. G. Vitali, who first described the PO from observations of the behaviour of PO-lesioned pigeons, proposed that this organ was needed to maintain normal wing muscle function and called it the 'organ of flight'. This interpretation has since been disputed. To solve this controversy and to test whether the PO is involved in flight and navigation, we performed release tests on homing pigeons subjected to bilateral destruction of this organ. No impairment of either flight or navigation was observed in the lesioned pigeons.

Homing behaviour of pigeons subjected to unilateral zinc sulphate treatment of their olfactory mucosa

Pigeons were made anosmic by unilateral treatment of their olfactory mucosa with a zinc sulphate solution and by plugging the contralateral nostril. In a series of releases at unfamiliar sites, 55­79 km from the home loft, the experimental birds' homing behaviour was compared with that of two control groups: unmanipulated control birds, and birds subjected to unilateral zinc sulphate treatment and equipped with an ipsilateral nasal plug. The experimental pigeons exhibited homing behaviour ­ in terms of both homeward initial orientation and homing performance ­ significantly poorer than that of both unmanipulated and treated control pigeons. In addition, the homing behaviour of the treated controls turned out to be only slightly, and not significantly, poorer than that of the unmanipulated birds. The results show that the impaired homing capabilities of the zinc-sulphate-treated birds are due to the lack of navigational information and not to non-specific brain damage caused by the experimental treatment.

Effects of ablation of the presumed equivalent of the mammalian prefrontal cortex on pigeon homing.

Pigeons (Columba livia) with bilateral ablation of the postero-dorsolateral neostriatum and the overlying corticoid were compared with unoperated control subjects in homing from both familiar and unfamiliar sites. Before the operation all the pigeons were subjected to 8 training flights from a site destined to be the familiar one. Postoperatively, the groups did not differ in orientation from the familiar site. In their releases from unfamiliar sites, however, the operated birds oriented in the training flight direction, whereas the control subjects were oriented homeward. In all the releases the homing performance, including both the homing speed and the number of returned birds, was significantly higher in the control group. Thus, the ablated tissue plays a role in homing behavior possibly through mediation of spatial orientation, of olfactory navigation, or of both.