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.
Although the optic tectum in non-mammals and its mammalian homolog, the superior colliculus, are involved in avoidance behaviors, whether and how tectal neurons respond to an object approaching on a collision course towards the animal remain unclear. Here we show by single unit recording that there exist three classes of looming-sensitive neurons in the pigeon tectal layer 13, which sends looming information to the nucleus rotundus or to the tectopontine system. The response onset time of tau cells is approximately constant whereas that for rho and eta cells depends on the square root of the diameter ⁄ velocity ratio of objects looming towards the animal, the cardioacceleration of which is also linearly related to the square root of this ratio. The receptive field of tectal cells is composed of an excitatory center and an inhibitory periphery, and this periphery does not inhibit responses to looming stimuli. These results suggest that three classes of tectal neurons are specified for detecting an object approaching on a collision course towards the animal, and that rho and eta cells may signal early warning of impending collision whereas tau cells initiate avoidance responses at a constant time before collision through the tectopontine system.
Misinterpretations of visual information received by the retina are called visual illusions, which are known to occur in higher brain areas. However, whether they would be also processed in lower brain structures remains unknown, and how to explain the neuronal mechanisms underlying the motion after-effect is intensely debated. We show by extracellular recording that all motion-sensitive neurons in the pigeon's pretectum respond similarly to real and illusory contours, and their preferred directions are identical for both contours in unidirectional cells, whereas these directions are changed by 90 deg for real versus illusory contours in bidirectional cells. On the other hand, some pretectal neurons produce inhibitory (excitatory) after-responses to cessation of prolonged motion in the preferred (null) directions, whose time course is similar to that of the motion after-effect reported by humans. Because excitatory and inhibitory receptive fields of a pretectal cell overlap in visual space and possess opposite directionalities, after-responses to cessation of prolonged motion in one direction may create illusory motion in the opposite direction. It appears that illusory contours and motion could be detected at the earliest stage of central information processing and processed in bottom-up streams, and that the motion after-effect may result from functional interactions of excitatory and inhibitory receptive fields with opposite directionalities.
The morphological characteristics of the pigeon lagena were examined using histology, scanning electron microscopy, and biotinylated dextran amine (BDA) neural tracers. The lagena epithelium was observed to lie partially in a parasagittal plane, but was also U-shaped with orthogonal (lateral) directed tips. Hair cell planar polarities were oriented away from a central reversal line that ran nearly the length of the epithelium. Similar to the vertebrate utricle and saccule, three afferent classes were observed based upon their terminal innervation pattern, which include calyx, dimorph, and bouton fibers. Calyx and dimorph afferents innervated the striola region of the lagena, while bouton afferents innervated the extrastriola and a small region of the central striola known as the type II band. Calyx units had large calyceal terminal structures that innervated only type I hair cells. Dimorph afferents innervated both type I and II hair cells, with calyx and bouton terminals. Bouton afferents had the largest most complex innervation patterns and the greatest terminal areas contacting many hair cells.
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