Arc Visualization of Odor Objects Reveals Experience-Dependent Ensemble Sharpening, Separation, and Merging in Anterior Piriform Cortex in Adult Rat

Abstract

Visualization using the immediate early gene Arc revealed sparser and more robust odor representations in the anterior piriform cortex of adult rats when odor was associated with water reward over 2-3 d. Rewarded odor "mixtures" resulted in rats responding to either component odor similarly, and, correspondingly, the odor representations became more similar as indexed by increased overlap in piriform Arc-expressing (Arc ϩ ) pyramidal neurons. The increased overlap was consistent with the rats' generalization from component odors. Discriminating among highly similar odor mixtures for reward led to increased differentiation of the neural representations as indexed by a reduction in overlap for piriform Arc ϩ pyramidal neurons after training. Similar odor mixture discrimination also required more trials to criterion. The visible reduction in the overlap of odor representations indexes pattern separation. The Arc visualization of odor representations in the anterior piriform network suggests that odor objects are widely distributed representations and can be rapidly modified by reward training in adult rats. We suggest that dynamic changes such as those observed here in piriform odor encoding are at the heart of perceptual learning and reflect the continuing plastic nature of mature associative cortex as an outcome of successful problem solving.

Locus coeruleus patterns differentially modulate learning and valence in ratviathe ventral tegmental area and basolateral amygdala respectively

“…A two-way mixed ANOVA revealed a significant effect of Day (F6, 66 = 10.713, p < 0.001), but no Group X Day interaction (F6, 66 = 0.755, p = 0.608), or Group effect (F1,11 = 0.527, p = 0.483). This underscores NE's role in discriminations that require pattern separation (5,9). Enhancement of subtle tactile discriminations by tonic 5-Hz LC activation (1) has also been reported in rats, a frequency not explored here.…”

Balancing the Robustness and Efficiency of Odor Representations during Learning

“…Previous studies have described learning-related plasticity at multiple levels within the olfactory system (Abraham et al, 2014; Chapuis and Wilson, 2012; Doucette and Restrepo, 2008; Doucette et al, 2011; Kass et al, 2013, 2016; Li et al, 2015; Shakhawat et al, 2014; Wachowiak et al, 2005). Our study contributes to the mounting evidence supporting the olfactory bulb as an important locus for learning- related activity changes (Abraham et al, 2014; Doucette and Restrepo, 2008; Doucette et al, 2011; Li et al, 2015).…”

“…These modulatory functions are sensitive to brain states, as neural activity in the olfactory bulb during the awake state has been shown to be dramatically different from the anesthetized state (Blauvelt et al, 2013; Kato et al, 2012; Kollo et al, 2014; Rinberg and Gelperin, 2006). Recent studies in awake behaving animals are beginning to shed light on the way olfactory experience and learning alters the dynamics of olfactory circuits (Abraham et al, 2014; Doucette and Restrepo, 2008; Doucette et al, 2011; Li et al, 2015; Shakhawat et al, 2014). However, a comprehensive understanding of how different types of experience affect odor representations in the early stages of processing is still lacking.…”

Learning modulation of odor representations: new findings from Arc-indexed networks

“…(C1) Odor reward learning increases the stability of the rewarded odor representation. S + refers to positive rewarded odor stimulus (e.g., peppermint); S − refers to negative unrewarded odor stimulus (e.g., vanillin; Shakhawat et al, 2014b ). When a trained rat is exposed to S + , the proportion of neurons recruiting Arc twice is increased.…”

“…It is temporally relocated from the nucleus, where it appears 5 min after recruitment, to cytoplasm where it asymptotes ~25 min later. Thus cells where Arc transcription is recently recruited by odor can be compared to the cells that responded to the same or a different odor at an earlier time point (Shakhawat et al, 2014a , b ).…”