A minimal magnetosensory circuit in the pigeon brain

The remarkable navigation abilities of the rock pigeon (Columba livia) are facilitated by a sensory system that allows the detection of magnetic fields. While there is compelling behavioral evidence demonstrating the existence of a magnetic sense, the neuronal circuits that process magnetic information in the brain are largely unknown, and the primary sensory cells and transduction molecules have yet to be identified. To address these issues, we combined tissue clearing and light sheet microscopy to screen the pigeon brain for magnetically induced neuronal activity via C-FOS expression. This screen revealed a minimal magnetosensory pathway that involves the central vestibular nuclei in the brainstem and the mesopallium, a multisensory integration center in the forebrain. These regions were robustly activated in magnetic experiments independently performed under white light and in total darkness. Building on these results, we investigated whether the receptive module of the magnetic sense is located in the vestibular system of the pigeon. Physical modelling suggests that the transduction mechanism of magnetoreception could rely on the detection of electric currents induced by magnetic fields in the semicircular canals of the pigeon. Consistent with this hypothesis, we report the presence of a splice isoform of the voltage-gated calcium channel CaV1.3, which is known to play a key role in electroreception, in sensory hair cells of the pigeon inner ear. The development of our screening platform and the identification of stably activated neuronal regions to magnetic stimuli will enable us to preform mechanistic experiments testing CaV1.3’s role in magnetoreception.