Facial whisker pattern is not sufficient to instruct a whisker-related topographic map in the mouse somatosensory brainstem

Abstract

Facial somatosensory input is relayed by trigeminal ganglion (TG) neurons and serially wired to brainstem, thalamus, and cortex. Spatially ordered sets of target neurons generate central topographic maps reproducing the spatial arrangement of peripheral receptors on the face. Facial pattern provides a template for map formation, but whether it is sufficient to impose a brain somatotopic pattern is unclear. In the mouse, lower jaw sensory information is relayed by the trigeminal nerve mandibular branch, whose axons target the brainstem dorsal principal sensory trigeminal nucleus (dPrV). Input from mystacial whiskers on the snout is relayed by the maxillary branch and form a topographic representation of rows and whiskers in the ventral principal trigeminal nucleus (vPrV). To investigate the importance of peripheral organisation in imposing a brain topographic pattern, we analysed the Edn1 mutant mice, in which lower-to-upper jaw transformation results in ectopic whisker rows on the lower jaw. In Edn1 mice, the lower jaw ectopic whiskers were innervated by mandibular TG neurons which initially targeted dPrV. Unlike maxillary TG neurons, the ectopic whisker-innervating mandibular neuron cell bodies and pre-target central axons did not segregate into a row-specific pattern nor targeted the dPrV with a topographic pattern. Following periphery-driven molecular repatterning to a maxillary-like identity, mandibular neurons redirected partially their central projections from dorsal to ventral PrV. Thus, a spatially ordered ectopic whisker pattern on the lower jaw is not sufficient to impose row-specific pre-target organization of the central mandibular tract nor a whisker-related matching pattern of afferents in dPrV, albeit still able to induce maxillary-like molecular features resulting in vPrV final targeting. These results provide novel insights into the relative importance of periphery-dependent versus periphery-independent mechanisms of trigeminal ganglion and brainstem patterning in matching facial whisker topography in the brainstem