Injury to structures in the central gustatory system such as the insula and operculum, the site of primary gustatory cortex in humans, can alter the flow of ascending and descending taste-related information through the brain which has great potential to disrupt normal gustatory processing and can have detrimental consequences on health and quality of life. As more advances are made in discerning the pharmacology, connectivity, and physiological phenotype of taste-responsive neurons in the brain, it is becoming increasingly critical for the field to develop and apply appropriate behavioral assays in animal models to explicitly link neurobiological processes to taste function. There is evidence in the literature that patients with damage involving primary gustatory cortex display hypogeusia and have difficulty identifying and recognizing tastes. In rats, lesions in the gustatory cortex retard, but do not eliminate, the acquisition of a conditioned taste aversion, retard acquisition of taste-based anticipatory contrast, and impair the expression of taste neophobia. In contrast, these lesions cause little, if any, effect on unconditioned taste preference and avoidance and do not disrupt taste preference conditioning. The prevailing view in the literature is that animals with gustatory cortex lesions display normal taste detection and discriminability, but, in actuality, this remains to be explicitly tested. Virtually all of the experiments on the effects of gustatory cortex lesions in rats have involved assessment of either conditioned or unconditioned affective/hedonic responsiveness to taste compounds. Moreover, with few exceptions, taste palatability has been assessed with intake and preference tests, which can be heavily influenced by postingestive factors and provide only a partial analysis of affective responsiveness. Thus, conclusions regarding the functional role of gustatory cortex are based on a relatively constrained set of behavioral observations. The goal of the proposed series of experiments is to fill this interpretive void by explicitly testing the necessity of the gustatory cortex in the maintenance of sensory-discriminative vs. affective taste function. Using a technically sophisticated apparatus (gustometer), we plan to test rats with and without ibotenic acid-induced lesions in the gustatory cortex in a variety of behavioral tasks designed to measure taste sensitivity (Exp. 1), taste quality discrimination (Exp.2 &3), the qualitative specificity of conditioned taste aversions (Exp. 3), and unconditioned affective responsiveness to taste stimuli as assessed by brief access licking tests (Exp. 4) and oromotor taste reactivity (Exp. 5). We predict that these lesions will blunt sensitivity and compromise the animal's ability to discriminate among taste stimuli that are used as sensory signals in psychophysical tasks, without affecting the palatability of the compounds. Regardless of the specific outcomes of these experiments, the data generated should provide a functional context in which to understand central gustatory processing.

Public Health Relevance

Impairments in the sense of taste can be very debilitating, adversely affecting the quality of life in such patients and jeopardizing their health. Moreover, given the role of taste in feeding and drinking, damage to the gustatory system can potentially contribute to more complex clinical disorders involving nutritional status, hydromineral balance, and obesity. The development of animal models, in which the gustatory system can be experimentally manipulated and the perceptual consequences assessed, is essential to gain an understanding of the underlying neurobiology of normal and abnormal taste function - a first step in refining the clinical management of patients suffering damage to gustatory brain sites and potentially leading to the development of therapeutic interventions.

National Institute of Health (NIH)
National Institute on Deafness and Other Communication Disorders (NIDCD)
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Special Emphasis Panel (ZRG1-IFCN-H (04))
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Sullivan, Susan L
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Florida State University
Schools of Arts and Sciences
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Spector, Alan C; le Roux, Carel W; Munger, Steven D et al. (2017) Proceedings of the 2015 ASPEN Research Workshop-Taste Signaling. JPEN J Parenter Enteral Nutr 41:113-124
Schier, Lindsey A; Spector, Alan C (2016) Behavioral Evidence for More than One Taste Signaling Pathway for Sugars in Rats. J Neurosci 36:113-24
Schier, Lindsey A; Blonde, Ginger D; Spector, Alan C (2016) Bilateral lesions in a specific subregion of posterior insular cortex impair conditioned taste aversion expression in rats. J Comp Neurol 524:54-73
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Blonde, Ginger D; Bales, Michelle B; Spector, Alan C (2015) Extensive lesions in rat insular cortex significantly disrupt taste sensitivity to NaCl and KCl and slow salt discrimination learning. PLoS One 10:e0117515
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King, Camille Tessitore; Hashimoto, Koji; Blonde, Ginger D et al. (2015) 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. Brain Res 1599:9-19
King, Camille Tessitore; Garcea, Mircea; Spector, Alan C (2014) 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. J Comp Neurol 522:2498-517
Schier, Lindsey A; Hashimoto, Koji; Bales, Michelle B et al. (2014) High-resolution lesion-mapping strategy links a hot spot in rat insular cortex with impaired expression of taste aversion learning. Proc Natl Acad Sci U S A 111:1162-7
Hashimoto, Koji; Spector, Alan C (2014) Extensive lesions in the gustatory cortex in the rat do not disrupt the retention of a presurgically conditioned taste aversion and do not impair unconditioned concentration-dependent licking of sucrose and quinine. Chem Senses 39:57-71