Having the nerve to home: trigeminal magnetoreceptor <i>versus</i>olfactory mediation of homing in pigeons

Gagliardo, Anna; Ioalè, Paolo; Savini, Maria; Wild, J. Martin

doi:10.1242/jeb.02313

Cited by 72 publications

(68 citation statements)

References 26 publications

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“…However, the results reported by Wiltschko et al actually speak against crucial involvement of the trigeminal system in navigation, as the anaesthetised pigeons showed unimpaired navigational abilities. This is consistent with what was reported in a series of experiments in which the V1 of homing pigeons were lesioned before release at unfamiliar sites (Gagliardo et al, 2006;Gagliardo et al, 2008;Gagliardo et al, 2009). In no case did lesioning V1 result in impairment in homing performance, and strikingly, birds with an intact V1 were unable to home if the olfactory nerve was severed.…”

Section: Introductionsupporting

confidence: 90%

A magnetic pulse does not affect homing pigeon navigation: a GPS tracking experiment

Holland

Filannino

Gagliardo

2013

Journal of Experimental Biology

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SUMMARYThe cues by which homing pigeons are able to return to a home loft after displacement to unfamiliar release sites remain debated. A number of experiments in which migratory birds have been treated with a magnetic pulse have produced a disruption in their orientation, which argues that a ferrimagnetic sense is used for navigation in birds. One previous experiment has also indicated an effect of magnetic pulses on homing pigeon navigation, although with inconsistent results. Previous studies have shown that some magnetic-related information is transmitted by the trigeminal nerve to the brain in some bird species, including the homing pigeon. The function of this information is still unclear. It has been suggested that this information is important for navigation. Previous studies with trigeminal nerve lesioned homing pigeons have clearly shown that the lack of trigeminally mediated information, even if magnetic, is not crucial for homing performance. However, this result does not completely exclude the possibility that other ferrimagnetic receptors in the homing pigeon play a role in navigation. Additionally, recent studies on homing pigeons suggested the existence of a ferrimagnetic sense in a novel location presumably located in the inner ear (lagena). In the present study, we tested whether any ferrimagnetic magnetoreceptors, irrespective of their location in the birdʼs head, are involved in pigeonsʼ homing. To do this, we treated homing pigeons with a strong magnetic pulse before release, tracked birds with GPS loggers and analyzed whether this treatment affected homing performance. In the single previous magnetic pulse experiment on homing pigeons, only initial orientation at a release site was considered and the results were inconsistent. We observed no effect of the magnetic pulse at any of the sites used on initial orientation, homing performance, tortuosity or track efficiency, which does not support a role for the ferrimagnetic sense in homing pigeon navigation, at least not in this geographic area, where magnetic field variations are in the region of 200nT intensity and 0.8deg inclination. Supplementary material available online at

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Section: Introductionsupporting

confidence: 90%

A magnetic pulse does not affect homing pigeon navigation: a GPS tracking experiment

Holland

Filannino

Gagliardo

2013

Journal of Experimental Biology

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“…Such procedures impair navigation even when visual cues are available (59). Although homing pigeons also orient by using geomagnetic fields (60), this input appears to be weighted less heavily than olfaction in experimentally displaced homing pigeons (61) and in migrating songbirds (62). Such experimental evidence for the primacy of olfactory inputs in navigation, across multiple diurnal bird orders, lends strong credence to the OS hypothesis.…”

Section: Birdsmentioning

confidence: 79%

From chemotaxis to the cognitive map: The function of olfaction

Jacobs

2012

Proc. Natl. Acad. Sci. U.S.A.

172

176

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A paradox of vertebrate brain evolution is the unexplained variability in the size of the olfactory bulb (OB), in contrast to other brain regions, which scale predictably with brain size. Such variability appears to be the result of selection for olfactory function, yet there is no obvious concordance that would predict the causal relationship between OB size and behavior. This discordance may derive from assuming the primary function of olfaction is odorant discrimination and acuity. If instead the primary function of olfaction is navigation, i.e., predicting odorant distributions in time and space, variability in absolute OB size could be ascribed and explained by variability in navigational demand. This olfactory spatial hypothesis offers a single functional explanation to account for patterns of olfactory system scaling in vertebrates, the primacy of olfaction in spatial navigation, even in visual specialists, and proposes an evolutionary scenario to account for the convergence in olfactory structure and function across protostomes and deuterostomes. In addition, the unique percepts of olfaction may organize odorant information in a parallel map structure. This could have served as a scaffold for the evolution of the parallel map structure of the mammalian hippocampus, and possibly the arthropod mushroom body, and offers an explanation for similar flexible spatial navigation strategies in arthropods and vertebrates.sensory | memory | orientation | limbic

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“…Mora et al (14) showed in a conditioning experiment that pigeons required intact ophthalmic branches of the trigeminal nerve (V1) to detect a strong magnetic anomaly, although Gagliardo et al (35)(36)(37) showed that V1 sectioned pigeons of all ages and levels of homing experience homed as well as control birds. Together, these results suggest that, although pigeons can detect magnetic information, V1 is not generally required for successful homing in this species.…”

Section: Discussionmentioning

confidence: 99%

Magnetic field changes activate the trigeminal brainstem complex in a migratory bird

Heyers

Zapka

Hoffmeister

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

117

124

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The upper beak of birds, which contains putative magnetosensory ferro-magnetic structures, is innervated by the ophthalmic branch of the trigeminal nerve (V1). However, because of the absence of replicable neurobiological evidence, a general acceptance of the involvement of the trigeminal nerve in magnetoreception is lacking in birds. Using an antibody to ZENK protein to indicate neuronal activation, we here document reliable magnetic activation of neurons in and near the principal (PrV) and spinal tract (SpV) nuclei of the trigeminal brainstem complex, which represent the two brain regions known to receive primary input from the trigeminal nerve. Significantly more neurons were activated in PrV and in medial SpV when European robins (Erithacus rubecula) experienced a magnetic field changing every 30 seconds for a period of 3 h (CMF) than when robins experienced a compensated, zero magnetic field condition (ZMF). No such differences in numbers of activated neurons were found in comparison structures. Under CMF conditions, sectioning of V1 significantly reduced the number of activated neurons in and near PrV and medial SpV, but not in lateral SpV or in the optic tectum. Tract tracing of V1 showed spatial proximity and regional overlap of V1 nerve endings and ZENK-positive (activated) neurons in SpV, and partly in PrV, under CMF conditions. Together, these results suggest that magnetic field changes activate neurons in and near the trigeminal brainstem complex and that V1 is necessary for this activation. We therefore suggest that V1 transmits magnetic information to the brain in this migratory passerine bird.bird migration | magnetic sense | magnetite | magnetoperception | magnetoreception

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Having the nerve to home: trigeminal magnetoreceptor versusolfactory mediation of homing in pigeons

Cited by 72 publications

References 26 publications

A magnetic pulse does not affect homing pigeon navigation: a GPS tracking experiment

A magnetic pulse does not affect homing pigeon navigation: a GPS tracking experiment

From chemotaxis to the cognitive map: The function of olfaction

Magnetic field changes activate the trigeminal brainstem complex in a migratory bird

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