Development of electrophysiological and morphological diversity in autonomic neurons

The generation of neuronal diversity requires the coordinated development o f differential patterns of ion channel expression along with characteristic differences in dendritic geometry, but the relations between these phenoty pic features are not well known. We have used a combination of intracellula r recordings, morphological analysis of dye-filled neurons, and stereologic al analysis of immunohistochemically labeled sections to investigate the de velopment of characteristic electrical and morphological properties of func tionally distinct populations of sympathetic neurons that project from the celiac ganglion to the splanchnic vasculature or the gastrointestinal tract of guinea pigs. At early fetal stages, neurons were significantly more dep olarized at rest compared with neurons at later stages, and they generally fired only a single action potential. By mid fetal stages, rapidly and slow ly adapting neurons could be distinguished with a topographic distribution matching that found in adult ganglia. Most rapidly adapting neurons (phasic neurons) at this age had a long afterhyperpolarization (LAH) characteristi c of mature vasomotor neurons and were preferentially located in the latera l poles of the ganglion, where most neurons contained neuropeptide Y. Most early and mid fetal neurons showed a weak M current, which was later expres sed only by rapidly-adapting and LAH neurons. Two different A currents were present in a subset of early fetal neurons and may indicate neurons destin ed to develop a slowly adapting phenotype (tonic neurons). The size of neur onal cell bodies increased at a similar rate throughout development regardl ess of their electrical or neurochemical phenotype or their topographical l ocation. In contrast, the rate of dendritic growth of neurons in medial reg ions of the ganglion was significantly higher than that of neurons in later al regions. The apparent cell capacitance was highly correlated with the su rface area of the soma but not the dendritic tree of the developing neurons . These results demonstrate that the well-defined functional populations of neurons in the celiac ganglion develop their characteristic electrophysiol ogical and morphological properties during early fetal stages of developmen t. This is after the neuronal populations can be recognized by their neuroc hemical and topographical characteristics but long before the neurons have finished growing. Our data provide strong circumstantial evidence that the development of the full phenotype of different functional classes of autono mic final motor neurons is a multi-step process likely to involve a regulat ed sequence of trophic interactions.