Taste Familiarity Is Inversely Correlated with Arc/Arg3.1 Hemispheric Lateralization

Abstract

Biochemical, electrophysiological, and imaging studies suggest that the anterior part of the insular cortex (IC) serves as primary taste cortex, whereas fMRI studies in human propose that the anterior IC is also involved in processing of general novelty or saliency information. Here, we compared activity regulated cytoskeleton associated protein (Arc)/Arg3.1 protein levels in the rat IC following administration of familiar versus novel tastes. Surprisingly, there was no correlation between novel taste and Arc/Arg3.1 levels when measured as the sum of both left and right insular cortices. However, when left and right IC were examined separately, Arc/Arg3.1 level was lateralized following novel taste learning. Moreover, Arc/Arg3.1 lateralization was inversely correlated with taste familiarity, whereas the high lateralization of Arc/Arg3.1 expression observed following novel taste learning is reduced proportionally to the increment in taste familiarity. In addition, unilateral inhibition of protein synthesis in the IC had asymmetrical effect on memory, inducing strong memory impairment similarly to bilateral inhibition or memory preservation, indicating that hemispheric lateralization is central for processing taste saliency information. These results provide indications, at the gene level of expression, for the role of IC lateralization in processing novel taste information and for the asymmetrical contribution of protein synthesis in each hemisphere during memory consolidation.

Sweet orosensation induces Arc expression in dorsal hippocampal CA1 neurons in an Experience‐dependent manner

“…That is, the combination of orosensation and postingestive consequences may be more efficient at inducing consolidation than orosensation alone, and that consequently, Arc expression decreases more slowly with repeated exposure to saccharin than with repeated exposure to sucrose. This interpretation is consistent with the recent finding that degree of saccharin experience does not impact saccharin-induced Arc protein expression in the gustatory cortex (Inberg et al, 2013).…”

LTD at amygdalocortical synapses as a novel mechanism for hedonic learning

“…There was a significant decrease in the number of c-Fos and EGR1 positive neurons following CTA ( Fig. 1d-f; c-Fos, control: 128.13 ± 9.46 positive nuclei/0.1mm 2 , N = 6, CTA: 82.21 ± 11.73 positive nuclei/0.1mm 2 , N = 6 rats, p < 0.01; EGR1, control: 175.90 ± 15.65 positive nuclei/0.1mm 2 , N = 6, CTA: 133.03 ± 10.10 positive nuclei/0.1mm 2 , N = 6, p < 0.05), suggesting that taste/malaise association decreased GC neurons activity, consistent with previous reports testing neuronal activity 2,12 and showing changes in markers for plasticity 10,13 .…”

The role of the gustatory cortex in incidental experience-evoked enhancement of later taste learning

“…prior to training, whereas the TPE effect is stronger following multiple presentations in the days prior to training; see for more discussion)] it is intriguing to think that TPE stimuli could induce plasticity related genes (Inberg et al 2013;Inberg et al 2016) that are similar to those identified in this earlier work, could act in the same way as behavioral tagging.…”

“…If so, perhaps inhibition induced immediately after TPE sessions (or a more molecular perturbation of plasticity such as protein synthesis inhibition, e.g. Ferreira et al 2005;Garcia-DeLaTorre et al 2009;Inberg et al 2013;Levitan et al 2016a) or even between taste deliveries would forestall the CTA enhancement observed here. It would be fascinating and valuable to test the time-course of this phenomenon across hours, as has been done in recent work on CTA consolidation (e.g., Levitan et al 2016a).…”

“…While much remains to be learned about this behavioral phenomenon, the above results do enable us to formulate basic hypotheses regarding how sensory taste information acquired during TPE is processed in the brain and integrated into future learning. An appropriate place to start in this regard is with primary gustatory cortex (GC), which resides in the anterior insula: GC has been amply shown, in electrophysiological studies (Katz et al 2001;Grossman et al 2008; Moran and Katz 2014;Sadacca et al 2016), immediate early gene imaging (Desmedt et al 2003;Contreras et al 2007;Inberg et al 2013;Uematsu et al 2015), and loss of function experiments (Berman and Dudai 2001;Stehberg and Simon 2011;Levitan et al 2016a;Levitan et al 2016b;Li et al 2016) to play a role in mediating taste behavior and CTA learning, as well as taste novelty/familiarity (Gallo et al 1992;Rosenblum et al 1993;Koh et al 2003;Bahar et al 2004;Koh and Bernstein 2005;Roman and Reilly 2007;Merhav and Rosenblum 2008;Nunez-Jaramillo et al 2008;Lin et al 2012c;Inberg et al 2013;Hadamitzky et al 2015). Here, we test the hypothesis that GC is vital for representing incidental taste experience and for driving the impact of that experience on later CTA learning.…”