Observing Magnetically-Mediated Behavior In Lab Mice
The ability of animals to sense the Earth’s magnetic field for spatial behaviors such as navigation and orientation is well-established. For example, the use of a magnetic compass has been demonstrated in many animal groups across different laboratories. Surprisingly, however, the sensory receptors and biophysical mechanisms mediating these responses are not fully understood.
In addition, the functional significance of some forms of magnetically mediated behavior is not intuitive and remains a topic of debate. For example, a wealth of vertebrate studies have provided evidence for spontaneous magnetic alignment behavior, in which animals exhibit an innate heading preference along the ~northeast-southwest magnetic axis. These subtle, yet widespread magnetically guided alignment preferences have led to the speculation that magnetic cues may play a more fundamental role in spatial ecology and cognition than previously realized.
In mammals, it remains to be determined if the type of magnetic response expressed (e.g. magnetic compass vs magnetic alignment) are species specific, or rather, if different forms of magnetic behavior can be exhibited within a species, perhaps reflecting the environmental, ecological or motivational context of the individual. Following a previously established magnetic compass training paradigm (Muheim et al. 2006), we trained laboratory mice to position nests in the direction corresponding to the dark end of a training cage aligned in one of four magnetic compass directions.
Mice were then placed individually inside a visually symmetrical circular arena under a natural or an experimentally shifted magnetic field alignment and allowed to construct a nest overnight. The following morning, the direction of the nest was determined (nests were measured relative to magnetic and geographic north). Overall, mice exhibited two distinct types of learned magnetic compass orientation that were dependent on the directional information learned during the training period, as well as spontaneous magnetic orientation that was independent of the trained direction. Interestingly, all three types of magnetic responses paralleled rather small, but seemingly important modifications to the training and/or testing protocols, suggesting that 1) magnetic behavior in mice is more flexible than previously thought, 2) magnetic responses appear to be context-dependent, and 3) the Earth’s magnetic field may play a larger role in spatial behavior than realized.
Specifically, we found that in the first phase of our study when mice were trained in a facility with electrical equipment located next to the training cages (e.g. heaters, air conditioners, dehumidifiers), that produced auditory and vibration disturbances, as well as intermittent radio-frequency noise, mice positioned nest sites along the northeast-southwest magnetic axis, independent of the intended trained magnetic direction. In other words, mice exhibited ‘non-learned’ spontaneous magnetic orientation.
One possibility is that the radio-frequency noise, which mice were intermittently exposed to during the training period, either prevented mice from learning magnetic information, or made this information less reliable or salient. Indeed, radio-frequency noise has been shown to disrupt magnetic responses across a range of vertebrate and invertebrate groups. However, we cannot rule out other possibilities that may be responsible for the spontaneous magnetic orientation responses exhibited by mice in this study (see Painter et al. 2018).
Shortly after, we moved the training setup into a separate room equipped with robust radio-frequency shielding (i.e. no radio-frequency noise was detected inside this training environment), and all electrical equipment was located in a separate room. Subsequently, mice began to exhibit learned magnetic compass orientation when tested following identical testing procedures as those used in the first phase of the study. Interestingly, and unlike responses published by Muheuim et al. 2006 where mice exhibited learned magnetic compass orientation corresponding to the sheltered end of the training cage, mice in this phase of our study positioned nests in directions corresponding to the light end of the cage (i.e. ~opposite than expected). Purely by chance, this phase of the experiment was performed during the summer months when ambient temperature and humidity steadily increased throughout the day.
Unlike the Muheium 2006 study, which established strict temperature and humidity criteria during testing, the environmental conditions in our test facility were not continually regulated throughout each test trail out of concern that the electrical equipment might disrupt behavioral responses. As a result, mice experienced a rapid increase in temperature and humidity over the span of each test. Therefore, we suggest that magnetic nest positioning towards the light end of the training cage is consistent with an ‘escape-like’ response reflecting the unsuitable environmental conditions in the testing facility.
In the last phase of the experiment, we designed an environmental circulation system in the test environment to continually regulate temperature and humidity, without exposing mice to increased acoustic, vibration, or radio-frequency disturbances. After this modification, mice exhibited learned magnetic compass orientation in the expected trained magnetic direction (i.e. in the direction corresponding to the sheltered end of the training cage).
Taken together, findings from the three phases of this study show that reliance on magnetic cues for nest positioning in laboratory mice can be influenced by a variety of factors, and may help to explain some of the difficulty in establishing or replicating magnetic responses in laboratory settings. Furthermore, these data provide evidence for plasticity in magnetic sensing in mammals, which opens up the possibility that magnetic cues may be used for more than just ‘simple’ compass information.
For example, the spontaneous magnetic alignment exhibited in the first phase of the study may reflect a more fundamental response to magnetic cues that helps to integrate magnetic and non-magnetic information when the animal finds itself in novel surroundings, as has been suggested previously. When mice did exhibit learned magnetic compass orientation, they were not simply learning the direction of the dark end of the training cage, but rather seemed to be encoding spatial relationships of their training environment relative to magnetic cues. Unlike simple compass information, encoding the spatial surroundings relative to some stable and reliable cue, such as the Earth’s magnetic field, would provide animals with rich and comprehensive spatial information about the environment to be used in a flexible, context-dependent manner.
These findings are described in the article entitled Evidence for plasticity in magnetic nest-building orientation in laboratory mice, recently published in the journal Animal Behaviour. This work was conducted by Michael S. Painter from Virginia Tech and the Czech University of Life Sciences, Madison Davis, Ella Rak, Kelsie Brumet, Hunter Bayne, and John B. Phillips from Virginia Tech, Shruthi Ganesh from the Virginia-Maryland College of Veterinary Medicine, and E. Pascal Malkemper from the Czech University of Life Sciences and University of Duisburg-Essen.