Absence of the Earths magnetic field activates stress-related brain circuits in a mammal

Abstract

The Earths magnetic field is a constantly available cue for animals with a magnetic sense. While magnetic navigation is best studied in migratory birds, a magnetic sense is also found in some mammals. Among these, it is most thoroughly studied in African mole-rats of the genus Fukomys, subterranean mammals that navigate in kilometre-long dark tunnel systems. Our understanding of the neural pathways involved in magnetoreception remains incomplete. To address this, we here performed an unbiased whole-brain screen for magnetically induced neuronal activity in the mole-rat brain. We set up MoBI-DisC (Mole-rat Brain Imaging with iDISCO and ClearMap), an experimental pipeline that combines global c-Fos immunolabelling, tissue clearing, light-sheet microscopy, and mapping to a novel 3D brain atlas. To identify brain areas involved in magnetosensation, we exposed mole-rats to a changing magnetic field and compared their brain activity to that of control animals exposed to a near-zero magnetic field. Unexpectedly, we found that the near-zero magnetic field exposure activated many brain areas, predominantly those involved in stress and anxiety responses. These included the amygdala, the bed nucleus of the stria terminalis, the substantia innominata, and the periaqueductal grey. This suggests that magnetic field deprivation acts as a physiological stressor in mole-rats. To test this, we conducted a place-preference test and found that mole-rats avoid entering a zone with a near-zero magnetic field, consistent with the hypothesis that this condition is not neutral for these animals. In summary, we present a novel pipeline for unbiased mapping of neural activity in subterranean mole-rats and uncover evidence of stress and avoidance responses to the absence of an Earth-strength magnetic field.