RESUMEN
Postingestive signals are important for shaping appetitive and consummatory responses, but the brain mechanisms required to assimilate interoceptive events with those at the frontlines of ingestion (taste-guided) are poorly understood. Here, we investigated whether an insular cortex (IC) region, which receives viscerosensory input, including gustatory, is required to modify taste-elicited consummatory reactions in response to a real-time interoceptive change using a serial taste reactivity (TR) test where the rats' oromotor and somatic reactions to intraoral (IO) infusions of sucrose were periodically assessed over 45 min following lithium chloride (LiCl) administration. Results showed that neurally-intact rats shifted from an ingestive repertoire to an aversive one as LiCl took effect. Overall, this hedonic shift was delayed in rats with bilateral neurotoxic IC lesions. Rats with greater neuronal loss in posterior gustatory IC displayed fewer aversive reactions to sucrose following this initial LiCl injection. We further assessed whether the failure to integrate interoceptive feedback with ongoing taste-guided behavior impaired acquisition and/or expression of conditioned aversion and/or avoidance in these same rats. Although, as a group, LiCl-injected rats with IC lesions subsequently avoided the sugar in a 48-h two-bottle test, their preference for sucrose was significantly greater than that of the LiCl-injected neurally-intact rats. Overall lesion size, as well as proportion of the posterior gustatory and/or anterior visceral IC were each associated with impaired avoidance. These findings reveal new roles for the posterior gustatory and anterior visceral ICs in multisensory integrative function.
Asunto(s)
Reacción de Prevención , Gusto , Animales , Reacción de Prevención/fisiología , Corteza Cerebral/fisiología , Condicionamiento Clásico/fisiología , Corteza Insular , Cloruro de Litio/farmacología , Ratas , Sacarosa , Gusto/fisiologíaRESUMEN
Rats display stereotypical oromotor and somatic responses to small volumes of intraorally infused taste solutions. These behaviors, known as taste reactivity, are categorized by their association with ingestion or rejection and are thought to reflect the palatability of the stimulus. Because supracollicular decerebrate rats display normal taste reactivity responses, it would appear that forebrain structures are not necessary for generating them. However, because moving the plane of transection rostrally, or damaging or manipulating specific ventral forebrain sites disrupts normal taste reactivity behavior, lesions of the gustatory cortex, a region that has been suggested to be involved with palatability processing, may do the same. In the current study, rats received two injections of either ibotenic acid (N=12) or vehicle (N=8), targeting the conventionally defined gustatory cortex in each hemisphere, and were implanted with intraoral cannulae. Following recovery, their responses to intraoral infusions (0.23ml in 1min) of dH2O, sucrose (1.0M and 0.1M), and quinine hydrochloride (3mM and 0.3mM) were video recorded. Analysis of brains with sufficient bilateral lesions (N=10) revealed that, on average, approximately 94% of the gustatory cortex was destroyed. These extensive bilateral lesions had no significant effect on taste reactivity; the numbers of ingestive and aversive responses to sucrose and quinine were similar between groups. Though these findings do not rule out involvement of the gustatory cortex in palatability processing, they make evident that the region of insular cortex destroyed is not necessary for the normal expression of unconditioned affective behavioral responses to taste stimuli.
Asunto(s)
Corteza Cerebral/fisiología , Conducta de Ingestión de Líquido/fisiología , Quinina/administración & dosificación , Sacarosa/administración & dosificación , Percepción del Gusto/fisiología , Gusto/fisiología , Animales , Catéteres de Permanencia , Corteza Cerebral/lesiones , Ácido Iboténico , Ratas Sprague-Dawley , Agua/administración & dosificaciónRESUMEN
Remarkably, when lingual gustatory nerves are surgically rerouted 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, even though 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 situated rostrally. 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 rostralmost CeA and in the subregion approximating the 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.
Asunto(s)
Núcleo Amigdalino Central/fisiología , Corteza Cerebral/fisiología , Nervio Lingual/fisiología , Regeneración Nerviosa/fisiología , Plasticidad Neuronal/fisiología , Percepción del Gusto/fisiología , Anastomosis Quirúrgica , Animales , Recuento de Células , Desnervación , Agua Potable/administración & dosificación , Inmunohistoquímica , Nervio Lingual/cirugía , Masculino , Neuronas/fisiología , Fotomicrografía , Estimulación Física , Proteínas Proto-Oncogénicas c-fos/metabolismo , Quinina/administración & dosificación , Ratas Sprague-Dawley , Gusto/fisiologíaRESUMEN
The distribution of quinine-stimulated Fos-like immunoreactivity (FLI) in several subdivisions of the parabrachial nucleus (PBN) known to be responsive to gustatory stimulation was examined in rats in which the chorda tympani nerve (CT) and/or glossopharyngeal nerve (GL) was transected (Experiment 1) and in rats in which the GL was transected with regeneration promoted or prevented (Experiment 2). We confirmed previous findings in the literature by demonstrating that rats intraorally infused with 3 mM quinine showed a robust population of FLI in the waist area and the external lateral (EL) and external medial (EM) subdivisions of the PBN (Yamamoto et al. [1994] Physiol Behav 56:1197-1202; Travers et al., [ 1999] Am J Physiol 277:R384-R394). In the waist area, only GL transection significantly decreased the number of FLI-neurons elicited by intraoral infusion of quinine compared with water-stimulated controls. In the external subdivisions neither neurotomy affected the number of FLI-neurons. The effect of GL transection in the waist area was enduring for rats in which the GL did not regenerate (up to 94 days), but regeneration of the GL after 52 days restored quinine-stimulated FLI to control values. In these same GL-transected animals, there were parallel decreases in the number of gapes elicited by intraoral quinine stimulation that recovered, but only subsequent to regeneration of the GL. These data provide support for the role of the waist area in the brainstem processing that underlies oromotor rejection behaviors and also help substantiate the hypothesis that the CT and GL are relatively specialized with regard to function. Moreover, when the quinine-induced pattern of neural activity in the second central gustatory relay, as assessed by FLI, is substantially altered by the loss of peripheral gustatory input from the GL, it can be restored upon regeneration of the nerve.