Developmental time course of peripheral cross‐modal sensory interaction of the trigeminal and gustatory systems

Abstract

Few sensory modalities appear to engage in cross-modal interactions within the peripheral nervous system, making the integrated relationship between the peripheral gustatory and trigeminal systems an ideal model for investigating cross-sensory support. The present study examined taste system anatomy following unilateral transection of the trigeminal lingual nerve (LX) while leaving the gustatory chorda tympani intact. At 10, 25, or 65 days of age, rats underwent LX with outcomes assessed following various survival times. Fungiform papillae were classified by morphological feature using surface analysis. Taste bud volumes were calculated from histological sections of the anterior tongue. Differences in papillae morphology were evident by 2 days post-transection of P10 rats and by 8 days post in P25 rats. When transected at P65, animals never exhibited statistically significant morphological changes. After LX at P10, fewer taste buds were present on the transected side following 16 and 24 days survival time and remaining taste buds were smaller than on the intact side. In P25 and P65 animals, taste bud volumes were reduced on the denervated side by 8 and 16 days post-surgery, respectively. By 50 days post-transection, taste buds of P10 animals had not recovered in size, however all observed changes in papillae morphology and taste buds subsided in P25 and P65 rats. Results indicate that LX impacts taste receptor cells and alters epithelial morphology of fungiform papillae, particularly during early development. These findings highlight dual roles for the lingual nerve in the maintenance of both gustatory and non-gustatory tissues on the anterior tongue.

Chronic Oral Capsaicin Exposure During Development Leads to Adult Rats with Reduced Taste Bud Volumes

“…It appears that the adult taste system is either able to maintain gustatory structures despite the presence of capsaicin or that capsaicin fails to cause damage in these animals. These results corroborate earlier evidence suggesting that the adult taste system is better able to withstand and recover from neural loss than the neonatal system (Sollars, 2005; Omelian et al, 2016). See Figure 5 for the distribution of adult taste bud volumes.…”

“…These time points were chosen to coincide with observed changes and regeneration in surgical studies (Sollars et al, 2002; Omelian et al, 2016). …”

“…Once tongues were removed, tissue was stored in an 8% paraformaldhyde solution. Taste bud volumes at the tongue tip have been shown to have a higher degree of size variability between buds than elsewhere on the anterior tongue (Krimm and Hill, 1998), thus the anterior-most 2 mm of the tongue tip was removed to allow for consistent volume measurements and to align with previous works (Krimm and Hill, 1998; Hendricks et al, 2004; Sollars et al, 2002; Sollars, 2005; Omelian et al, 2016). Tissue was then frozen and 300 coronal, serial sections (10 µm, each) were obtained using a cryostat, and sections were mounted on gel-coated slides.…”

“…In order to be consistent with previous literature (e.g., Krimm & Hill, 1998; Mistretta et al, 1999; Hendricks et al, 2004; Shuler et al, 2004; Sollars, 2005; Omelian et al, 2016) taste bud volumes were combined within treatment group, each consisting of 4 animals and 134–153 total taste buds per group. One-way ANOVAs with a Tukey post hoc test were run to assess within group variance, and identify any outliers (for ANOVA results, see Table 1).…”

“…It is notable that changes in taste buds following CTX occur concurrently with morphological changes to the lingual-innervated papillae themselves, despite the fact that the CT does not directly innervate the papilla proper. Loss of the lingual nerve exclusively (i.e., leaving the CT intact) also produces developmentally differential effects in which younger animals undergo greater reductions in taste bud count and volume, as well as disrupted papillae morphology (Omelian et al, 2016). In total, the outcomes following either gustatory or trigeminal nerve transection suggest that while the CT and lingual nerves are distinctly different in location and function, an integrated, multimodal relationship exists between the taste and trigeminal systems in the anterior tongue.…”