Evolutionary divergence of trigeminal nerve somatotopy in amniotes

Abstract

The trigeminal circuit relays somatosensory input from the face into the central nervous system. In central nuclei, the spatial arrangement of neurons reproduces the physical distribution of peripheral receptors, thus generating a somatotopic facial map during development. In mice, the ophthalmic, maxillary, and mandibular trigeminal nerve branches maintain a somatotopic segregation and generate spatially organized patterns of connectivity within hindbrain target nuclei. To investigate conservation of somatotopic organization, we compared trigeminal nerve organization in turtle, chick, and mouse embryos. We found that, in the turtle, mandibular and maxillary ganglion neuron rostrocaudal segregation and trigeminal tract somatotopy are similar to mouse. In contrast, chick mandibular ganglion neurons are located rostrally to maxillary neurons, with some intermingling, supporting previous observations (Noden [1980], J Comp Neurol 190:429-444). This organization results in an inversion of the relative positions and less precise axonal sorting of the maxillary and mandibular branches within the trigeminal tract, as compared to mouse and turtle. Moreover, using the turtle and chick orthologs of Drg11 in combination with Hoxa2 expression and axonal tracings from the periphery, we mapped the chick PrV nucleus position to rhombomere 1, confirming previous studies (Marin and Puelles [1995], Eur J Neurosci 7:1714-1738) and in contrast to mouse PrV, which mainly maps to rhombomere 2-3 (Oury et al. [2006], Science 313:1408-1413). Thus, somatotopy of trigeminal ganglion and nerve organization is only partially conserved through amniote evolution, possibly in relation to the modification of facial somatosensory structures and morphologies.

Organotopic organization of the primary Infrared Sensitive Nucleus (LTTD) in the western diamondback rattlesnake (Crotalus atrox)

“…A prominent area of overlap with fibers from the mandibular branch and both maxillar branches that innervate the pit organ of the upper jaw in these animals was found in central areas of the LTTD (Molenaar, ). This anatomical pattern of afferent fiber terminations is completed by inputs from the ophthalmic branch to ventral areas of the LTTD, compatible with the current findings in pit vipers and the organization of the common trigeminal system of reptiles in general (Rhinn et al, ). The presence of areas in the LTTD with overlapping projections from the pit organs of the lower and upper jaws in pythons might be explained by the fact that certain regions of both pit organs have a matching spatial correspondence of environmental cues, potentially explaining a central convergence of signals from the respective areas of the dual pit organs that benefits from common termination areas.…”

Development and Functional Organization of the Cranial Nerves in Lampreys

“…The central distribution pattern of these fibers was studied by specific HRP application to the five different trigeminal nerves (Koyama et al, ). Curiously, the somatotopic organization of trigeminal sensory fibers is similar to that found in some gnathostomes (see Rhinn et al, ), with the maxillary branch (V2) projecting dorsally, the ophthalmic branch (V1) projecting ventrally, and the mandibular branch (V3) projecting laterally (Koyama et al, ). This organization, however, appears to be inverted in the hagfish Eptatretus burgeri (Nishizawa et al, ).…”

Identification of molecular signatures specific for distinct cranial sensory ganglia in the developing chick

“…The validity of the marker sets was confirmed by considering genes whose expression has been shown previously to be restricted to specific cranial sensory ganglia. Thus trigeminal ophthalmic expressed PAX3 [ 10 , 28 , 29 ]; trigeminal maxillomandibular/ophthalmic ganglia expressed DRG11 [ 30 – 32 ]; and nodose/petrosal ganglia expressed PHOX2B [ 11 , 21 , 33 – 35 ]. Our panel of markers included 7 genes expressed in the nodose ganglion but not in the petrosal ganglion.…”