Primary Sensory Neuron Addition in the Adult Rat Trigeminal Ganglion: Evidence for Neural Crest Glio-Neuronal Precursor Maturation

It is debated whether primary sensory neurons of the dorsal root ganglia increase the number in adult animals and, if so, whether the increase is attributable to postnatal neurogenesis or maturation of dormant, postmitotic precursors. Similar studies are lacking in the trigeminal ganglion (TG). Here we demonstrate by stereological methods that the number of neurons in the TG of adult male rats nearly doubles between the third and eighth months of age. The increase is mainly attributable to the addition of small, B-type neurons, with a smaller contribution of large, A-neurons. We looked for possible proliferative or maturation mechanisms that could explain this dramatic postnatal expansion in neuron number, using bromodeoxyuridine (BrdU) labeling, immunocytochemistry for neural precursor cell antigens, retrograde tracing identification of peripherally projecting neurons, and in vitro isolation of precursor cells from adult TG explant cultures. Cell proliferation identified months after an extended BrdU administration was sparse and essentially corresponded to glial cells. No BrdU-labeled cell took up the peripherally injected tracer, and only a negligible number coexpressed BrdU and the pan-neuronal tracer neuron-specific enolase. In contrast, a population of cells not recognizable as mature neurons in the TG and neighboring nerve expressed neuronal precursor antigens, and neural crest glioneuronal precursor cells were successfully isolated from adult TG explants. Our data suggest that a protracted maturation process persists in the TG that can be responsible for the neuronal addition found in the adult rat.