Extensive Lesions in Rat Insular Cortex Significantly Disrupt Taste Sensitivity to NaCl and KCl and Slow Salt Discrimination Learning

Abstract

While studies of the gustatory cortex (GC) mostly focus on its role in taste aversion learning and memory, the necessity of GC for other fundamental taste-guided behaviors remains largely untested. Here, rats with either excitotoxic lesions targeting GC (n = 26) or sham lesions (n = 14) were assessed for postsurgical retention of a presurgically LiCl-induced conditioned taste aversion (CTA) to 0.1M sucrose using a brief-access taste generalization test in a gustometer. The same animals were then trained in a two-response operant taste detection task and psychophysically tested for their salt (NaCl or KCl) sensitivity. Next, the rats were trained and tested in a NaCl vs. KCl taste discrimination task with concentrations varied. Rats meeting our histological inclusion criterion had large lesions (resulting in a group averaging 80% damage to GC and involving surrounding regions) and showed impaired postsurgical expression of the presurgical CTA (LiCl-injected, n = 9), demonstrated rightward shifts in the NaCl (0.54 log10 shift) and KCl (0.35 log10 shift) psychometric functions, and displayed retarded salt discrimination acquisition (n = 18), but eventually learned and performed the discrimination comparable to sham-operated animals. Interestingly, the degree of deficit between tasks correlated only modestly, if at all, suggesting that idiosyncratic differences in insular cortex lesion topography were the root of the individual differences in the behavioral effects demonstrated here. This latter finding hints at some degree of interanimal variation in the functional topography of insular cortex. Overall, GC appears to be necessary to maintain normal taste sensitivity to NaCl and KCl and for salt discrimination learning. However, higher salt concentrations can be detected and discriminated by rats with extensive damage to GC suggesting that the other resources of the gustatory system are sufficient to maintain partial competence in these tasks, supporting the view that such basic sensory-discriminative taste functions involve distributed processes among central gustatory structures.

Bilateral lesions in a specific subregion of posterior insular cortex impair conditioned taste aversion expression in rats

“…Similarly, one of the nine rats categorized as having primarily extensive IC 3 damage, with little IC 2 damage, was relatively impaired on all CTA tests. Although the general picture that is emerging from our recently published work Schier et al, 2014;Blonde et al, 2015) points to a more complex functional topography of GC and IC, findings that encourage the use and comprehensive analysis of more targeted lesions, the highresolution lesion-mapping approach employed here, have also begun to underscore the possible incidence of anatomical variation between individual rat brains. In fact, Hashimoto and Spector (2014) first reported the relatively considerable intersubject and interhemispheric variability in the relative position of the intersection of the middle cerebral artery and the rhinal fissure (see also Kida et al, 2015).…”

“…Although lesion studies have traditionally revealed a critical role for GC in CTA (see, e.g., Braun et al, ; Lasiter and Glanzman, ; Dunn and Everitt, ; Bermudez‐Rattoni and McGaugh, ; Nerad et al, ; Cubero et al, ; Fresquet et al, ; Roman and Reilly, ), several recent reports have questioned this attribution (Geddes et al, ; Hashimoto and Spector, , Schier et al, ; Blonde et al, ). Indeed, a previous study in rats from our laboratory failed to find evidence of CTA impairment following extensive damage in GC (Schier et al, ).…”

“…Incidentally, Blonde et al () also found that a group of rats with extensive bilateral lesions that conjointly encompassed the majority of the GC and the posterior region of IC identified by Schier et al () exhibited CTA deficits to a sucrose taste stimulus in a postsurgical brief‐access test. These lesions also impeded NaCl and KCl taste sensitivity as assessed psychophysically in separate two‐response operant tests and slowed the acquisition rate of an NaCl vs. KCl taste discrimination, but these particular deficits were not correlated with the CTA deficits.…”

Overlapping representation of primary tastes in a defined region of the gustatory cortex

“…Moreover, this area is targeted in most awake recording studies, linking taste responses to behavioral function (Katz et al, 2001;Fontanini and Katz, 2008;Samuelsen et al, 2012;Maier and Katz, 2013). Lesions centered in this area have effects on quinine and salt, but not sucrose, sensitivity and discrimination Blonde et al, 2015).…”

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

“…Using a two‐response operant task that requires immediate responses to very small volumes of stimuli, thus minimizing postingestive contributions, our lab previously showed that large, bilateral lesions in GC (~80% on average) impaired normal taste detection for NaCl and KCl. 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.…”