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

PLOS ONE, Dec 2019

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.

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

February Extensive Lesions in Rat Insular Cortex Significantly Disrupt Taste Sensitivity to NaCl and KCl and Slow Salt Discrimination Learning Ginger D. Blonde 0 1 2 3 Michelle B. Bales 0 1 2 3 Alan C. Spector 0 1 2 3 0 Funding: This study was supported by the National Institute on Deafness and Other Communication Disorders: R01-DC-DC009821 (ACS); T32-DC- 000044 (MBB). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript 1 Data Availability Statement: All relevant data are within the paper 2 Academic Editor: Sidney Arthur Simon, Duke University Medical Center , UNITED STATES 3 Department of Psychology and Program in Neuroscience, Florida State University , Tallahassee, FL , United States of America 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. - Competing Interests: The authors have declared that no competing interests exist. The gustatory cortex (GC) is conventionally defined as a zone of agranular/dysgranular insular cortex flanking the middle cerebral artery containing taste-responsive neurons [17], and has been a focus for studying taste aversion learning and memory in the rat. Bilateral lesions to GC are reported to virtually eliminate the retention of a presurgically conditioned taste aversion (CTA), in which animals are trained to avoid a tastant by pairing its ingestion with visceral malaise [2; 812]. Similarly, postsurgical acquisition is often, but not always, impaired [8 9,11,1321]. The effects of pharmacological manipulations during CTA induction also suggest involvement of GC in taste memory consolidation [2225]. However, recent findings from our laboratory, while confirming that insular cortex lesions compromise CTA learning, question whether the critical site encompasses GC alone or rather also involves adjacent sites implicated in visceroception [26]. Interestingly, intake tests suggest that unconditioned preference and avoidance appear normal under most, but not all, test conditions after GC damage [9, 2729]. In agreement, extensive bilateral damage to GC has little effect on unconditioned concentration-dependent responsiveness to sucrose or quinine [30]. Collectively, these prior studies suggest that GC is unnecessary for normal unconditioned hedonic responsiveness to tastants and that its role in taste aversion learning may be in conjunction with visceroceptive areas of insular cortex. This raises the question as to the functional role of GC. An early hypothesis by Pfaffmann and colleagues (1977) postulated that the thalamocortical gustatory pathway provides information regarding stimulus identification and discriminability, while the divergent ventral forebrain gustatory pathway is involved in tasteguided motivation and affect [31]. However, despite evidence suggesting that humans experience hypogeusia and difficulty identifying tastes after damage to insular cortex [3235], whether (...truncated)


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Ginger D. Blonde, Michelle B. Bales, Alan C. Spector. Extensive Lesions in Rat Insular Cortex Significantly Disrupt Taste Sensitivity to NaCl and KCl and Slow Salt Discrimination Learning, PLOS ONE, 2015, 2, DOI: 10.1371/journal.pone.0117515