Extensive Gustatory Cortex Lesions Significantly Impair Taste Sensitivity to KCl and Quinine but Not to Sucrose in Rats

Abstract

Recently, we reported that large bilateral gustatory cortex (GC) lesions significantly impair taste sensitivity to salts in rats. Here we extended the tastants examined to include sucrose and quinine in rats with ibotenic acid-induced lesions in GC (GCX) and in sham-operated controls (SHAM). Presurgically, immediately after drinking NaCl, rats received a LiCl or saline injection (i.p.), but postsurgical tests indicated a weak conditioned taste aversion (CTA) even in controls. The rats were then trained and tested in gustometers to discriminate a tastant from water in a two-response operant taste detection task. Psychometric functions were derived for sucrose, KCl, and quinine. Our mapping system was used to determine placement, size, and symmetry of the lesions (~91% GC damage on average). For KCl, there was a significant rightward shift (ΔEC50 = 0.57 log10 units; p<0.001) in the GCX psychometric function relative to SHAM, replicating our prior work. There was also a significant lesion-induced impairment (ΔEC50 = 0.41 log10 units; p = 0.006) in quinine sensitivity. Surprisingly, taste sensitivity to sucrose was unaffected by the extensive lesions and was comparable between GCX and SHAM rats. The fact that such large bilateral GC lesions did not shift sucrose psychometric functions relative to SHAM, but did significantly compromise quinine and KCl sensitivity suggests that the neural circuits responsible for the detection of specific taste stimuli are partially dissociable. Lesion-induced impairments were observed in expression of a postsurgical CTA to a maltodextrin solution as assessed in a taste-oriented brief-access test, but were not reflected in a longer term 46-h two-bottle test. Thus, deficits observed in rats after extensive damage to the GC are also dependent on the test used to assess taste function. In conclusion, the degree to which the GC is necessary for the maintenance of normal taste detectability apparently depends on the chemical and/or perceptual features of the stimulus.

Opioid and orexin hedonic hotspots in rat orbitofrontal cortex and insula

“…However, damage to those higher structures would produce loss of hierarchical control but not loss of original functions remaining in lower structures. These considerations may help explain why cortical lesions of the hedonic hotspot/coldspot sites identified here have generally failed to impair measures of food reward (12,14,61,64). Similarly, human patients with extensive damage to OFC and insula appear to remain capable of normal hedonic reactions to many pleasant versus unpleasant stimuli (9,10).…”

“…However, the role of the cortex as necessary for "liking" is questioned by evidence that cortical damage usually does not cause loss of hedonic function: Lesions in the OFC, insula, or anterior cingulate cortex in humans do not reliably suppress positive hedonic reactions to many pleasant stimuli, despite causing cognitive impairments that alter decisions about selection, pursuit, and consumption of rewards (7)(8)(9)(10)(11). Similarly in animal studies, cortical lesions fail to strongly suppress reward-elicited behaviors (12)(13)(14).Showing that the cortex causes gains of function in the motivation to consume food rewards, Mena et al (15) recently reported that cortical mu-opioid stimulation in rats, via microinjections of DAMGO, a synthetic opioid agonist with high mu-opioid receptor selectivity, in the medial prefrontal cortex (PFC) produced robust increases of food intake. Here, we aimed to assess whether similar opioid stimulations in the prefrontal and insula cortex might also specifically cause increases in the hedonic impact of the sensory pleasure of food, as assessed by orofacial "liking" reactions to sweetness.Beyond opioid stimulation, orexin stimulation has been found to similarly cause "liking" enhancements in the same NAc and VP hotspots where DAMGO enhances hedonic impact (16, 17), raising the possibility that any cortical opioid hotspot for "liking" enhancement might also be stimulated by orexin.…”

“…However, the role of the cortex as necessary for "liking" is questioned by evidence that cortical damage usually does not cause loss of hedonic function: Lesions in the OFC, insula, or anterior cingulate cortex in humans do not reliably suppress positive hedonic reactions to many pleasant stimuli, despite causing cognitive impairments that alter decisions about selection, pursuit, and consumption of rewards (7)(8)(9)(10)(11). Similarly in animal studies, cortical lesions fail to strongly suppress reward-elicited behaviors (12)(13)(14).…”

Chemospecific deficits in taste sensitivity following bilateral or right hemispheric gustatory cortex lesions in rats

“…The same lesions retarded the acquisition of a NaCl versus KCl discrimination, even though it was eventually learned (Blonde, Bales, & Spector, 2015). Bales, Schier, Blonde, and Spector (2015) replicated the impairment in KCl detection in rats with large bilateral lesions in GC (~91% damage) and these same rats also displayed a modest rightward shift in sensitivity to quinine, but, surprisingly, they displayed absolutely no impairment in the detection of sucrose.…”

“…Anatomical landmarks distinctly associated with one brain section, according to the rat brain atlas (Paxinos & Watson, 2007), were used to determine the best approximate AP coordinate (see Bales et al, 2015; Table 2). The AP distance between the landmarks as seen in the atlas was divided by the number of sections between those landmarks for each brain.…”