Optical mapping reveals the functional organization of the trigeminal nuclei in the chick embryo

The functional organization of the trigeminal nuclei during embryogenesis w as investigated using multiple-site optical recording with a fast voltage-s ensitive dye. Brainstem preparations, with three classified trigeminal nerv e afferents, the ophthalmic, maxillary and mandibular nerves, together with motor nerve fibers, were dissected from five- to eight-day-old chick embry os. Electrical responses evoked by trigeminal nerve stimulations were optic ally recorded simultaneously from many loci of the stained preparations. We identified three response areas related to the trigeminal nerve: area I, l ocated cephalic to the level of the trigeminal ganglion; area II, located c audal to the level of the trigeminal ganglion; and area III, located at the level of the trigeminal root. The neural responses in areas I and II were evoked by ophthalmic, maxillary or mandibular nerve stimulation, while the responses in area In were detected when the stimulation was applied to the trigeminal motor nerve. In comparison with the morphology indicated by DiI labeling, the results suggest that areas I, II and In correspond to the pri ncipal sensory nucleus of the trigeminal nerve, the spinal sensory nucleus of the trigeminal nerve and the trigeminal motor nucleus, respectively. We identified two components of the optical response: a fast and a slow signal . In five-day-old preparations, fast spike-like signals related to action p otentials were recorded from the three response areas. In six-day-old prepa rations, slow optical signals which reflect glutamate-mediated excitatory p ostsynaptic potentials were detected from area II, only when the ophthalmic nerve was stimulated: no slow signal was evoked by maxillary or mandibular nerve stimulation In seven- and eight-day-old preparations, slow signals w ere detected from both areas I and II with every nerve stimulation. These r esults suggest that synaptic function is first generated in the spinal trig eminal nucleus by the six-day embryonic stage, and the developmental organi zation of synaptic function is not the same in the three trigeminal nerves or in the two sensory nuclei. Contour line maps of the signal amplitude rev ealed that the size and the area of the neural responses within the trigemi nal nuclei changed dramatically with development. We compared the spatial d istribution and temporal dynamics of the optical signals between the ophtha lmic, maxillary and mandibular nerve stimulations, and we found that somato topic organization is less clear in a rostrocaudal/mediolateral X-Y plane, although the areas of the maxillary and mandibular nerves appeared to separ ate in the lateral direction. (C) 1999 IBRO. Published by Elsevier Science Ltd.