Regenerative Failure Following Rat Neonatal Chorda Tympani Transection is Associated with Geniculate Ganglion Cell Loss and Terminal Field Plasticity in the Nucleus of the Solitary Tract

Abstract

Neural insult during development results in recovery outcomes that vary dependent upon the system under investigation. Nerve regeneration does not occur if the rat gustatory chorda tympani nerve is sectioned (CTX) during neonatal (≤ P10) development. It is unclear how chorda tympani soma and terminal fields are affected after neonatal CTX. The current study determined the impact of neonatal CTX on chorda tympani neurons and brainstem gustatory terminal fields.To assess terminal field volume in the nucleus of the solitary tract (NTS), rats received CTX at P5 or P10 followed by chorda tympani label, or glossopharyngeal (GL) and greater superficial petrosal (GSP) label as adults. In another group of animals, terminal field volumes and numbers of chorda tympani neurons in the geniculate ganglion (GG) were determined by labeling the chorda tympani with DiI at the time of CTX in neonatal (P5) and adult (P50) rats. There was a greater loss of chorda tympani neurons following P5 CTX compared to adult denervation.Chorda tympani terminal field volume was dramatically reduced 50 days after P5 or P10 CTX.Lack of nerve regeneration after neonatal CTX is not caused by ganglion cell death alone, as approximately 30% of chorda tympani neurons survived into adulthood. Although the total field volume of intact gustatory nerves was not altered, the GSP volume and GSP-GL overlap increased in the dorsal NTS after CTX at P5, but not P10, demonstrating age-dependent plasticity. Our findings indicate that the developing gustatory system is highly plastic and simultaneously vulnerable to injury. Highlights• The volume of chorda tympani central processes is severely diminished after the nerve is sectioned in 5-or 10-day-old rats.• Compared to adult injury, neonatal denervation produced greater loss of terminal field and ganglion cell bodies.• About 30% of chorda tympani neurons survive early section, suggesting lack of regeneration is not caused by cell loss alone.• The organization of intact gustatory terminal fields is altered by early chorda tympani nerve section.2004; Reddaway et al., 2012), but it is not clear how the CT itself is impacted by neonatal CTX.The present study was designed to determine the effects of neonatal CTX on CT neurons and intact nerve terminal fields of the GL and GSP. To examine this, gustatory nerve terminal fields were labeled following neonatal CTX, and CT neurons in the GG were examined after neonatal or adult CT denervation. We found that neonatal CTX caused a profound loss of CT terminal field and ganglion cells and altered the organization of intact gustatory terminal fields. Experimental Procedures SubjectsFemale Sprague-Dawley rats (n = 47) were used for these experiments. Rats were bred in the University of Nebraska at Omaha vivarium. The day of birth was designated P0, and animals were weaned at P25. Rats were socially housed in clear Plexiglas cages where they had free access to food pellets (Teklad or Labdiet) and tap water. Animals were kept on a 12:12 light-dark cycle. All procedures were approve...

Terminal field volume of the glossopharyngeal nerve in adult rats reverts to prepruning size following microglia depletion with PLX5622

“…The NTS and solitary tract were visualized using phase contrast (Martin et al., 2019; Riquier & Sollars, 2020). The intermediate zone was classified as one section before and after solitary tract passes through the rostral‐most portion of the NTS, for a total of three sections (150 µm; Riquier & Sollars, 2017, 2020).…”

“…The unit of analysis was always one animal, with the sample size for each analysis expressed as n . Sample sizes were estimated based on our previous studies in rats examining NTS microglia (Riquier & Sollars, 2017, 2020) and NTS terminal fields (Martin et al., 2019). All data were treated as independent/between‐subjects factors for analyses, and no collected data were omitted.…”