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Rapid Learning of Magnetic Compass Direction by C57BL/6 Mice in a 4-Armed ‘Plus’ Water Maze

PLOS
PLOS ONE
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Magnetoreception has been demonstrated in all five vertebrate classes. In rodents, nest building experiments have shown the use of magnetic cues by two families of molerats, Siberian hamsters and C57BL/6 mice. However, assays widely used to study rodent spatial cognition (e.g. water maze, radial arm maze) have failed to provide evidence for the use of magnetic cues. Here we show that C57BL/6 mice can learn the magnetic direction of a submerged platform in a 4-armed (plus) water maze. Naïve mice were given two brief training trials. In each trial, a mouse was confined to one arm of the maze with the submerged platform at the outer end in a predetermined alignment relative to magnetic north. Between trials, the training arm and magnetic field were rotated by 180(°) so that the mouse had to swim in the same magnetic direction to reach the submerged platform. The directional preference of each mouse was tested once in one of four magnetic field alignments by releasing it at the center of the maze with access to all four arms. Equal numbers of responses were obtained from mice tested in the four symmetrical magnetic field alignments. Findings show that two training trials are sufficient for mice to learn the magnetic direction of the submerged platform in a plus water maze. The success of these experiments may be explained by: (1) absence of alternative directional cues (2), rotation of magnetic field alignment, and (3) electromagnetic shielding to minimize radio frequency interference that has been shown to interfere with magnetic compass orientation of birds. These findings confirm that mice have a well-developed magnetic compass, and give further impetus to the question of whether epigeic rodents (e.g., mice and rats) have a photoreceptor-based magnetic compass similar to that found in amphibians and migratory birds.
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... Besides bats (e. g. Holland et al. 2006, Wang et al. 2007), magnetic compass orientation has been documented in several subterranean mole-rats (Burda et al. 1990, Kimchi & Terkel 2001, Oliveriusová et al. 2012, as well as in small rodents active above ground: the Siberian hamster (Deutschlander et al. 2003), the inbred C57BL/6J mouse (Muheim et al. 2006, Phillips et al. 2013, the bank vole (Oliveriusová et al. 2014) and the wood mouse doi: 10.37520/lynx.2022.017 (Malkemper et al. 2015). ...
... More recent studies, however, suggest that the magnetic compass of epigeic rodents shares some important features with birds rather than with mole-rats. Most importantly, their compass seems to need blue light and is sensitive to magnetic fields oscillating in the MHz range (Muheim et al. 2006, Phillips et al. 2013, Malkemper et al. 2015, a diagnostic property of a radical pair-based mechanism (Ritz et al. 2004). Whether the magnetic compass of epigeic rodents exhibits also other functional characteristics that are typical for the avian magnetic compass remains unknown. ...
... Although conducted overnight, nest building experiments that demonstrated magnetic compass orientation in laboratory mice, hamsters and wood mice (see Introduction) invariably started with a period of time during which the experimental animals were allowed to explore the arena under natural (Malkemper et al. 2015) or artificial white light (Deutschlander et al. 2003, Muheim et al. 2006. Likewise, the water maze experiments in which mice were successfully trained to remember the magnetic compass direction of a submersed platform were performed under white light (Phillips et al. 2013). For now, it remains unclear whether light influences rodents' motivation or primary magnetoreception events. ...
Article
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Our knowledge about magnetoreception in mammals remains limited. Among rodents, magnetic compass orientation has been documented in four subterranean mole-rats and four epigeic (i.e., active above ground) species. While it is well established that the magnetic compass of mole-rats is light-independent and magnetite-mediated, recent evidence suggests that a radical pair-based mechanism may underlie magnetic orientation in epigeic rodents. To determine whether the magnetic compass of epigeic rodents is light-dependent, which is thought to be an inherent feature of radical pair-based magnetoreception, we investigated the ability of the bank vole Clethrionomys glareolus (Cricetidae) to use magnetic compass orientation in total darkness. The voles, which were allowed to explore/build a nest overnight in a circular arena, did not exhibit any directional preference in the initial stage of the experiments; later they tended to prefer the southern sector of the arena irrespective of magnetic field direction, implying that they relied on nonmagnetic orientation cues. Previous tests (Oliveriusová et al. 2014) in the same environment, but under lighting, showed a significant reaction to a change in the orientation of the magnetic field. On the basis of the presented study in comparison with the previous one, it can be concluded that bank voles do not use the magnetic compass for near-space orientation in darkness and thus support evidence for light-dependent magnetoreception in a mammal.
... Magnetic compass orientation has been convincingly demonstrated in only several species: in bats (e.g. Holland et al. 2006, 2010, Wang et al. 2007, subterranean rodents (Burda et al. 1990, Kimchi & Terkel 2001, Oliveriusová et al. 2012) and epigeic rodents: the Siberian hamster (Deutschlander et al. 2003), the inbred C57BL/6J mouse (Muheim et al. 2006, Phillips et al. 2013, the bank vole (Oliveriusová et al. 2014), and the wood mouse (Malkemper et al. 2015). But in the naked mole-rats, the results could be considered display of magnetosensitivity only (Malewski et al. 2018). ...
... Recently a new method has appeared to study magnetic compass orientation more efficiently (Phillips et al. 2013). A four-arm "plus" water maze was used for forced learning. ...
... After successful test of magnetic orientation in the bank vole (Oliveriusová et al. 2014), we decided to use for a new orientation test the water maze according to Phillips et al. (2013). For our studies, the previous (Oliveriusová et al. 2014), as well as the just presented, we Phillips et al. (2013). ...
Article
A long-term issue when studying magnetic orientation is the replicability of the experiments conducted in different laboratories. Attempts to replicate experiments have failed many times. After our previous study where we successfully found magnetoreception in the bank vole (Clethrionomys glareolus) we decided to replicate the water maze experiment. The bank voles were trained and tested in a four-arm “plus” maze in different magnetic conditions – natural magnetic field and three magnetic fields with shifted position of magnetic north (+90°, +180°, and +270°). The tested bank voles showed learned directional preference in the water maze therefore we can consider this species magnetoreceptive, able to use magnetic field for orientation. However, the results were more scattered than in the study with C57BL/6J mice. This difference probably corresponds with the absence of the protection against disturbing radio frequency magnetic fields during experiment, as well as, with the behavioural differences of free-living voles and laboratory mice.
... The directional preference of each bird was calculated as the vector sum of the time spent in the four arms during the 90 s probe trial without food reward (see "Methods" for details on the data analysis). The use of this symmetrical testing format makes it possible to partition the variability in the distribution of bearings into an 'absolute' or 'topographic' component, a 'spontaneous magnetic' or 'untrained magnetic' component, and a 'trained magnetic' component 7,51 . In the absence of a response to the magnetic field, the resulting distributions from the group of birds tested under the same experimental condition were uniformly distributed (i.e., indistinguishable from random; see distributions of responses exhibited by birds exposed to broadband RF fields in training and/or testing). ...
... The orientation of an individual bird was calculated from the time (number of frames) it spent in each of the four maze arms during the 90 s trial (cf. 10,51 ). The topographic directions of the four maze arms, i.e. 0°, 90°, 180°, and 270°, weighed by the number of frames the bird spent in each of the arms, were added using vector addition, which resulted in a topographic mean orientation for the individual bird 60 . ...
Article
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The avian magnetic compass can be disrupted by weak narrow-band and broadband radio-frequency (RF) fields in the lower MHz range. However, it is unclear whether disruption of the magnetic compass results from the elimination of the perception pattern produced by the magnetic field or from qualitative changes that make the pattern unrecognizable. We show that zebra finches trained in a 4-arm maze to orient relative to the magnetic field are disoriented when tested in the presence of low-level (~ 10 nT) Larmor-frequency RF fields. However, they are able to orient when tested in such RF fields if trained under this condition, indicating that the RF field alters, but does not eliminate, the magnetic input. Larmor-frequency RF fields of higher intensities, with or without harmonics, dramatically alter the magnetic compass response. In contrast, exposure to broadband RF fields in training, in testing, or in both training and testing eliminates magnetic compass information. These findings demonstrate that low-level RF fields at intensities found in many laboratory and field experiments may have very different effects on the perception of the magnetic field in birds, depending on the type and intensity of the RF field, and the birds’ familiarity with the RF-generated pattern.
... The directional preference of each bird was calculated as the vector sum of the time spent in the four arms during the 90 s probe trial without food reward (see Methods for details on the data analysis). The use of this symmetrical testing format makes it possible to partition the variability in the distribution of bearings into an 'absolute' or 'topographic' component, a 'spontaneous magnetic' or 'untrained magnetic' component, and a 'trained magnetic' component 7,51 . In the absence of a response to the magnetic eld, the resulting distributions from the group of birds tested under the same experimental condition were uniformly distributed (i.e., indistinguishable from random; see distributions of responses exhibited by birds exposed to broadband RF elds in training and/or testing). ...
... The orientation of an individual bird was calculated from the time (number of frames) it spent in each of the four maze arms during the 90 s trial (cf. 10,51 ). The topographic directions of the four maze arms, i.e. 0°, 90°, 180°, and 270°, weighed by the number of frames the bird spent in each of the arms, were added using vector addition, which resulted in a topographic mean orientation for the individual bird 57 . ...
Preprint
Full-text available
The avian magnetic compass can be disrupted by weak narrow-band and broadband radio-frequency (RF) fields in the lower MHz range. However, it is unclear whether disruption of the magnetic compass results from the elimination of the perception pattern produced by the magnetic field or from qualitative changes that make the pattern unrecognizable. We show that zebra finches trained in a 4-arm maze to orient relative to the magnetic field are disoriented when tested in the presence of low-level (~ 10 nT) Larmor-frequency RF fields. However, they are able to orient when tested in such RF fields if trained under this condition, indicating that the RF field alters, but does not eliminate, the magnetic input. Larmor-frequency RF fields of higher intensities, with or without harmonics, dramatically alter, the magnetic compass response. In contrast, exposure to broadband RF fields in training, in testing, or in both training and testing eliminates magnetic compass information. These findings demonstrate that low-level RF fields at intensities found in many laboratory and field experiments may have very different effects on the perception of the magnetic field in birds, depending on the type and intensity of the RF field, and the birds’ familiarity with the RF-generated pattern.
... It is unknown what kinds of sensory mechanisms large terrestrial mammals use for their navigation performance. However, in smaller mammals it has been shown that olfactory 23 , visual 24 and magnetic cues 25 can be used for orientation. In principle, larger mammals, such as the red deer (Cervus elaphus), can use all of these cues, if available. ...
Article
Full-text available
Many animals return to their home areas (i.e., ‘homing’) after translocation to sites further away. Such translocations have traditionally been used in behavioral ecology to understand the orientation and migration behavior of animals. The movement itself can then be followed by marking and recapturing animals or by tracking, for example, using GPS systems. Most detailed studies investigating this behavior have been conducted in smaller vertebrates (e.g., birds, amphibians, and mice), whereas information on larger mammals, such as red deer, is sparse. We conducted GPS-assisted translocation experiments with red deer at two sites in the Czech Republic. Individuals were translocated over a distance of approximately 11 km and their home journey was tracked. Circular statistics were used to test for significant homeward orientation at distances of 100, 500, 1000, and 5000 m from the release site. In addition, we applied Lavielle trajectory segmentation to identify the different phases of homing behavior. Thirty-one out of 35 translocations resulted in successful homing, with a median time of 4.75 days (range 1.23–100 days). Animals were significantly oriented towards home immediately after release and again when they came closer to home; however, they did not show a significant orientation at the distances in between. We were able to identify three homing phases, an initial ‘exploratory phase’, followed by a ‘homing phase’ which sometimes was again followed by an ‘arrival phase’. The ‘homing phase’ was characterized by the straightest paths and fastest movements. However, the variation between translocation events was considerable. We showed good homing abilities of red deer after translocation. Our results demonstrate the feasibility of conducting experiments with environmental manipulations (e.g., to impede the use of sensory cues) close to the release site. The homing behavior of red deer is comparable to that of other species, and might represent general homing behavior patterns in animals. Follow-up studies should further dissect and investigate the drivers of the individual variations observed and try to identify the sensory cues used during homing.
... In reptiles, the dominant role of magnetic compass for orientation was reliably demonstrated mainly over much larger distances, e.g., in transoceanic migration of loggerhead turtles (Lohmann et al. 2001, Fuxjager et al. 2011 or during spontaneous magnetic alignments (Landler et al. 2015, Diego-Rasilla et al. 2017. Interestingly, learning to navigate in adapted 4-armed (plus) water maze according to the alignment with magnetic north, that was experimentally changed between the trials was very efficient in mice (Phillips et al. 2013). The animals learn the magnetic direction of the submerged platform only after two training trials. ...
Article
Full-text available
The spatial orientation of mammals and birds has been intensively studied for many years, but the cognitive mechanism of spatial orientation used by squamates remains less well understood. In our study, we evaluated the learning abilities of leopard geckos, Eublepharis macularius (Blyth, 1854) in an adapted Morris Water Maze (MWM) with access to proximal and distal cues. We experimentally manipulated the number of reliable arena cues and one distinct room cue. The animals learned during the training phase as well as during the cue manipulation phase. No manipulation with proximal or distal cues caused loss of orientation for the entire group. The animals were able to switch between navigation strategies and showed individual preferences for the different cues. The individual geckos attend to a combination of proximal and distal cues and flexibly adjust their strategy when some of the cues are missing, which is indicative of allothetic orientation. However, the motivation of geckos for solving the task and the quality of learned spatial information were highly individual.
... As mentioned in a previous paper (Balmori, 2016), laboratory scientists investigating the orientation of animals know there is a need to shield the place at which the experiments are performed, in order to prevent interference from man-made radiation, as anthropogenic signals may distort the results (Vacha et al., 2009;Wiltschko et al., 2014;Phillips et al., 2022;Muheim and Phillips, 2023). In the absence of such precautions (for example, filters covering a wide range of frequencies), the sensitivity to low-level radiofrequency fields at levels found in typical laboratory environments may be a source of unexplained variability when the spatial movements of animals are studied (Phillips et al., 2013;2022). However, field scientists investigating animal movements and other aspects of animal ecology are equipping animals with radio transmitters that emit the same type of pulsed radiofrequency radiation (Mech and Barber, 2002). ...
Article
Any study carried out with a given technique must avoid causing harmful effects on the experimental subjects, in order to avoid altering the survival rates of the animals or causing bias in the results of the study. Radio tagging is undoubtedly a very useful technique, and in many cases is the only option available to obtain information on the ecology and movements of wild animals, but unfortunately it has been used indiscriminately, without regard to the problems it can cause. The most well-known of these are the effects from the weight of the device and the harness, but there are others that have not yet been taken into account and that have not been sufficiently studied, such as the non-thermal effects of modulated and/or pulsed electromagnetic fields on the health and orientation of radio-tracked animals. This commentary provides a brief overview of the scientific evidence on the effects of electromagnetic fields, and underlines the importance of carrying out relevant studies in order to check for the possible effects of radio transmitters on animals.
... It is unknown what kind of sensory mechanisms large terrestrial mammals use for their navigation performance. However, in smaller mammals it has been shown that olfactory [23], visual [24] and magnetic cues [25] can be used for orientation. In principle, larger mammals, such as the red deer (Cervus elaphus), could use all of these cues if available. ...
Preprint
Full-text available
Background Many animals move back to their home area (i.e., ‘homing’) after translocation to sites further away. Such translocations have traditionally been used in behavioral ecology to understand orientation and migration behavior of animals. The movement itself can then be followed by marking and recapturing of animals or by tracking, e.g., using GPS systems. Most detailed studies investigating this behavior were conducted with smaller vertebrates (e.g., birds, amphibians and mice), whereas information on larger mammals, such as red deer, is sparse. Methods We conducted GPS assisted translocation experiments with red deer at two sites in the Czech Republic. Individuals were translocated over a distance of about 11 km and their home journey was tracked. We used circular statistics to test for significant homeward orientation at 100, 500, 1000 and 5000 m distance to the release site. In addition, we applied a Lavielle trajectory segmentation, identifying different phases of the homing behavior. Results Thirty-one out of 35 translocations resulted in successful homing with a median time of 4.75 days (range: 1.23 to 100 days). Animals significantly oriented towards home immediately after release and again when they came closer to home; however, they did not show significant orientation at the distances in between. We were able to identify three homing phases, an initial ‘exploratory phase’, followed by a ‘homing phase’ which sometimes was again followed by an ‘arrival phase’. The ‘homing phase’ was characterized by the straightest paths and fastest movements. However, variation between translocation events was considerable. Conclusions We show good homing abilities of red deer after translocation. Our results show the feasibility to conduct experiments with environmental manipulations (e.g., to impede the use of sensory cues) close to the release site. The homing behavior of red deer is comparable to other species and might represent general homing behavior patterns in animals. Follow up studies should further dissect and investigate the drivers of the individual variations we observed, and try to identify the sensory cues used during homing.
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The unusual capacity of some tropical freshwater fishes (of the dominating subgroup Teleostei) to generate and sense electric signals, the discharges of their weak electric organs, was discovered by Hans Lissmann (1951, 1958) of the University of Cambridge. He demonstrated the function of an active elec-trolocation system, but, along with others, also proposed a second function, that of communication. Studies in electrical communication were pioneered by Patricia Black-Cleworth (1970), then in the laboratory of T. Bullock at the University of California in La Jolla, and Peter Moller (1970), then in the laboratory of T. Szabo at the CNRS research institute and the Collège de France in Paris.
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