Restoration of quinine‐stimulated fos‐immunoreactive neurons in the central nucleus of the amygdala and gustatory cortex following reinnervation or cross‐reinnervation of the lingual taste nerves in rats

Abstract

Remarkably, when lingual gustatory nerves are surgically re-routed to inappropriate taste fields in the tongue, some taste functions recover. We previously demonstrated that quinine-stimulated oromotor rejection reflexes and neural activity (assessed by Fos-immunoreactivity) in subregions of hindbrain gustatory nuclei were restored if the posterior tongue, which contains receptor cells that respond strongly to bitter compounds, was cross-reinnervated by the chorda tympani nerve. Such functional recovery was not seen if instead, the anterior tongue, where receptor cells are less responsive to bitter compounds, was cross-reinnervated by the glossopharyngeal nerve, despite that this nerve typically responds robustly to bitter substances. Thus, recovery depended more on the taste field being reinnervated than on the nerve itself. Here, the distribution of quinine-stimulated Fos-immunoreactive neurons in two taste-associated forebrain areas was examined in these same rats. In the central nucleus of the amygdala (CeA), a rostrocaudal gradient characterized the normal quinine-stimulated Fos response, with the greatest number of labeled cells rostrally situated. Quinine-stimulated neurons were found throughout the gustatory cortex but a ‘hot spot’ was observed in its anterior-posterior center in subregions approximating the dysgranular/agranular layers. Fos neurons here and in the rostral CeA were highly correlated with quinine-elicited gapes. Denervation of the posterior tongue eliminated, and its reinnervation by either nerve restored, numbers of quinine-stimulated labeled cells in the rostral-most CeA and in the subregion approximating dysgranular gustatory cortex. These results underscore the remarkable plasticity of the gustatory system and also help clarify the functional anatomy of neural circuits activated by bitter taste stimulation.

Unconditioned oromotor taste reactivity elicited by sucrose and quinine is unaffected by extensive bilateral damage to the gustatory zone of the insular cortex in rats

“…As an example, using the TR procedure in combination with Fos immunohistochemistry, we recently observed more quinine- than water-stimulated neural activity throughout the rostrocaudal extent of the GC (King et al, 2014). That transection of both the glossopharyngeal nerve and the chorda tympani nerve attenuated the numbers of quinine-stimulated Fos-neurons and their regeneration restored them confirmed that the neural response was taste-mediated and not due to postingestive stimulation (King et al, 2014). Of particular relevance to the current study, significant correlations ( r = 0.65 to r = .75) between the numbers of quinine-stimulated gapes and Fos positive neurons in regions approximating DI and AI throughout GC were found.…”

Behavioral analyses of taste function and ingestion in rodent models

“…Camille King, when she was a postdoc in my lab, and Mircea Garcea, extended Joe’s work and showed that, in the absence of the glossopharyngeal nerve, the chorda tympani nerve could maintain normal gaping to quinine, if it was cross-regenerated into the posterior tongue (Figure 6) [34]. In fact, this profile of responding emulated the profile seen for Fos activation throughout the central gustatory system [34, 35]. …”

Genetic recombination in disgust-associated bitter taste-responsive neurons of the central nucleus of amygdala in male mice

“…Since a rostrocaudal gradient characterized the quinine-stimulated cFos response, with the greatest number of labeled cells situated rostrally in the CeA [7], the rostral and middle levels of the CeA along the rostrocaudal axis, which corresponds to the CeA from Bregma level -0.70 to -1.46 [39], were analyzed.…”

“…The disgust reactions are associated with cFos expression, a marker of neuronal activity, in several brain regions such as the external part of the medial parabrachial nucleus, nucleus of the solitary tract [6], rostral part of the central nucleus of the amygdala (CeA), insular cortex [7] and interstitial nucleus of the posterior limb of the anterior commissure (IPAC) [8]. These brain regions appear to consist of functionally heterogeneous neurons [9][10][11][12][13][14].…”

“…While the quinine-activated disgust-associated neurons in the IPAC are preferentially accessible by a targeted recombination in active populations (TRAP) method [8,19], it remains unclear whether the accessibility is restricted to the IPAC or not. It is interesting to investigate whether the quinine-activated neurons in the CeA [7] are accessible by TRAP because of the following reasons: (1) the CeA is one of the well-known emotional centers but its role in the disgust reactions remains unclear; (2) the CeA consists of functionally heterogeneous neurons, and the expression of a single molecular marker and Cre transgenics in the molecularly defined neurons likely cannot capture the functional heterogeneity in the CeA [13,20,21]; (3) the CeA neurons are not successfully TRAPed by any stimuli [19,[22][23][24][25][26][27][28][29][30][31][32]; (4) the CeA and the IPAC, where a significant number of neurons were successfully TRAPed by quinine infusion [8], are directly continuous anatomically and are grouped as a part of the distinct anatomical division, the central division of the extended amygdala [9].…”