Magnetic field-driven induction of ZENK in the trigeminal system of pigeons ( Columba livia )

Abstract

Magnetoreception remains one of the few unsolved mysteries in sensory biology. The upper beak, which is innervated by the ophthalmic branch of the trigeminal nerve (V1), has been suggested to contain magnetic sensors based on ferromagnetic structures. Recently, its existence in pigeons has been seriously challenged by studies suggesting that the previously described iron-accumulations are macrophages, not magnetosensitive nerve endings. This raised the fundamental question of whether V1 is involved in magnetoreception in pigeons at all. We exposed pigeons to either a constantly changing magnetic field (CMF), to a zero magnetic field providing no magnetic information, or to CMF conditions after V1 was cut bilaterally. Using immediate early genes as a marker of neuronal responsiveness, we report that the trigeminal brainstem nuclei of pigeons, which receive V1 input, are activated under CMF conditions and that this neuronal activation disappears if the magnetic stimuli are removed or if V1 is cut. Our data suggest that the trigeminal system in pigeons is involved in processing magnetic field information and that V1 transmits this information from currently unknown, V1-associated magnetosensors to the brain.

Eyes are essential for magnetoreception in a mammal

“…This would be consistent with the finding of magnetically induced neural activity in a part of the Ansell's mole-rat's superior colliculus that predominantly receives trigeminal input (Němec et al, 2001). The trigeminal nerve has further been demonstrated to be involved in the magnetic sense in birds (Heyers et al, 2010, Lefeldt et al, 2014, but the exact location and structure of avian trigeminal magnetoreceptors is equally unknown (Engels et al, 2018).…”

Experienced migratory songbirds do not display goal-ward orientation after release following a cross-continental displacement: an automated telemetry study

“…Recent displacement studies provide support for this hypothesis in songbirds2021. Magnetoreceptors associated with the ophthalmic branch of the trigeminal nerve have been suggested as likely candidates allowing birds to sense positional information222324, although this has been debated25.…”

Sensory mechanisms of long-distance navigation in birds: a recent advance in the context of previous studies

“…Given the controversy around the magnetite magnetoreceptors in the upper beak region (Edelman et al 2014;Fleissner et al 2007;Treiber et al 2012), and, at the same time, the growing body of neurophysiological and behavioural data strongly supporting the existence of a magnetic sensor associated with the trigeminal nerve (Beason et al 1996;Heyers et al 2010;Kishkinev et al 2013;Lefeldt et al 2014;Mora et al 2004; the magnetic pulsing studies), a method suitable for visualisation of these magnetic receptors in the beak region is desperately needed; (b) If an iron mineral magnetoreceptor is identified, we need to describe its cellular and intracellular structure and propose the mechanisms of magnetic field sensing; (c) Reveal the role of specific geomagnetic parameters for positioning. To do that, virtual displacement experiments are needed when specific magnetic parameters are changed while other ones are left intact.…”

“…One should mention here that a very similar experimental approach failed to condition European robins and a few other passerine species for the discrimination of magnetic cues (Kishkinev et al 2012). Recent studies by Heyers et al (2010) and Lefeldt et al (2014) using European robins and homing pigeons strongly suggest that the avian trigeminal nerve transmits magnetic input into the brain, though an intact trigeminal nerve is neither necessary nor enough for magnetic compass orientation (Beason and Semm 1996;Zapka et al 2009). These studies strongly suggest that trigeminal nerve endings should innervate magnetic receptors.…”