Magnetoreception in an avian brain in part mediated by inner ear lagena

Abstract

Many animals use the Earth's geomagnetic field for orientation and navigation, but the neural mechanisms underlying that ability remain enigmatic. Support for at least two avian magnetoreceptors exists, including magnetically activated photochemicals in the retina and ferrimagnetic particles in the beak. The possibility of a third magnetoreceptor in the inner ear lagena organs has been suggested. The brain must process magnetic receptor information to derive constructs representing directional heading and geosurface location. Here, we used the c-Fos transcription factor, a marker for activated neurons, to discover where in the brain computations related to a specific set of magnetic field stimulations occur. We found that neural activations in discrete brain loci known to be involved in orientation, spatial memory, and navigation may constitute a major magnetoreception pathway in birds. We also found, through ablation studies, that much of the observed pathway appears to receive magnetic information from the pigeon lagena receptor organs.

Figure 1

Magnetic field stimulation. a) Schematic illustration of rotating (360° azimuth plane) magnetic field vector (red arrow) for 12 different elevations (blue-green lines). Thirty-six different vector planes were used for each stimulation, 12 directed along each of the X (shown), Y, and Z axes, referenced to the head-centered pigeon.

Figure 2

Photomicrographs and anatomical tracings for c-Fos positive neurons. a–d) Images arranged in columns for the vestibular nuclei, dorsal thalamus, hippocampus, and hyperpallium (left – right), for four stimulus conditions including Mag3x (a), Rest (b), Sham surgery (c), and lagena Lesion (d). C-Fos positive neurons identified by dark stained nuclei (immunolabel bound to the expressed c-Fos protein) are clearly visible, with the highest activation patterns exhibited in the Mag3x and Sham condition birds. Reconstructions of transverse sections with activated neurons (black dots) in the posterior vestibular nuclei (left column), dorsal thalamus (middle column), and hippocampus and dorsal hyperpallium (right column). Counting frames (boxes) used for quantification of activated cell counts are indicated. D, descending vestibular nucleus; DLP, dorsolateral posterior thalamic n.; DIP, dorsointermediate posterior thalamic n.; DMP, dorsomedial posterior thalamic n.; HA, hyperpallium apicale; HD, hyperpallium densocellulare; Hp, hippocampus; IO, inferior olivary n.; M, medial vestibular nucleus; MD; dorsal mesopallium; N, nidopallium; OT, optic tectum; ST, nucleus of the solitary tract; XII, hypoglossal n.; IX–X, glossopharyngeal and vagal motor nuclei.. Scale bar = 500 μm for (a–d). Scale bars in (e) as indicated.

Figure 3

Number of activated cells for different brain regions and stimulus conditions. a) Mean number of activated neurons for all birds in the vestibular nuclei, dorsal thalamus, hippocampus, and hyperpallium for Mag3x (black), Sham (gray), Mag1x (dark gray), Rest (light gray), and lagena Lesion (light black) conditions. b) Mean values (propagation error formula) for Magnetic field only (Mag3x – Rest) and Lagena only (Mag3x – lagena Lesion) mean number of cells. Error bars = ±SEM.

Figure 4

Mag3x and lagena Lesion anatomical tracings. Transverse sections with all activated cells plotted (red dots) as to location to yield the neural distributions in representative birds for Mag3x (left column) and lagena Lesion (right column) conditions. Sections are arranged in rostral-to-caudal order, distances relative to AP0 (interaural axis). CbL, lateral cerebellar n.; CbM, medial cerebellar n.; GP, globus pallidus; IC, inferior colliculus; L, lateral vestibular nucleus; LA, lateral anterior thalamic n.; nBOR, n. of the basal optic root; PoA, amygdaloid complex; PrV, principal trigeminal n.; IV, forth ventricle; S, superior vestibular n. Other abbreviations as in Fig 2.