Distinct Progressions of Neuronal Activity Changes Underlie the Formation and Consolidation of a Gustatory Associative Memory

Abstract

Acquiring new memories is a multistage process. Numerous studies have convincingly demonstrated that initially acquired memories are labile and are stabilized only by later consolidation processes. These multiple phases of memory formation are known to involve modification of both cellular excitability and synaptic connectivity, which in turn change neuronal activity at both the single neuron and ensemble levels. However, the specific mapping between the known phases of memory and the changes in neuronal activity at different organizational levels-the single-neuron, population representations, and ensemblestate dynamics-remains unknown. Here we address this issue in the context of conditioned taste aversion learning by continuously tracking gustatory cortex neuronal taste responses in alert male and female rats during the 24 h following a taste-malaise pairing. We found that the progression of activity changes depends on the neuronal organizational level: whereas the population response changed continuously, the population mean response amplitude and the number of taste-responsive neurons only increased during the acquisition and consolidation phases. In addition, the known quickening of the ensemble-state dynamics associated with the faster rejection of harmful foods appeared only after consolidation. Overall, these results demonstrate how complex dynamics in the different representational levels of cortical activity underlie the formation and stabilization of memory within the cortex.

LiCl-induced sickness modulates rat gustatory cortical responses

“…In addition to altering μ power, LiCl also significantly altered GC taste responses. This fact dovetails nicely with data presented by Arieli and colleagues [ 85 ], who examined how GC activity changes following CTA learning, identifying 2 types of impact resulting from the pairing of taste with LiCl-induced illness—an “immediate” impact of LiCl administration on taste responses in GC single neurons and a “delayed” impact on GC ensemble population dynamics in taste response. Arieli and colleagues hypothesized that the late impact is driven by CTA formation, and that the immediate impact is likely caused by the illness state induced by LiCl injection.…”

Taste Experience Enhances Cortical Response Reliability during Latent Enhancement of Taste Aversion Learning

“…These results indicate that taste experience specifically reduces the response variability during the palatability epoch-the epoch known to be critically impacted during CTA learning (Grossman et al, 2008;Moran and Katz, 2014;Arieli et al, 2022). Consistent with behavioral work showing enhanced learning with low conditioned stimulus variation (e.g., Jennings and Bonardi, 2017), the increase in across-trial reliability we see here may well make it easier for the rats to learn CTA.…”

“…Ensemble (neuron-to-neuron) response reliability during CTA conditioning. While many statistical algorithms have been applied to detect state transitions in neural spiking data (e.g., hidden Markov Modeling, Jones et al, 2007), here we used Bayesian Changepoint Analysis (BCA) to determine the presence of sudden, coherent firing-rate transitions in ensemble taste responses, which have been shown to exist in taste responses (Katz et al, 2001;Jones et al, 2007;Sadacca et al, 2012) and to be relevant to both naïve behavior (Li et al, 2016;Sadacca et al, 2016) and CTA learning (Grossman et al, 2008;Moran and Katz, 2014;Arieli et al, 2022). Unlike many other methods that provide a single point estimate through maximum likelihood estimation, we chose BCA because, as demonstrated below, it offers a distribution of parameter estimates.…”

Cortical Coding of Gustatory and Thermal Signals in Active Licking Mice

“…For the first question, we can safely speculate that these oral signals are integral to flavor processing and behavioral responses, particularly in relation to consummatory behavior. The gustatory cortex has been implicated in functions related to taste processing (Katz et al, 2001; Blonde et al, 2015; Sadacca et al, 2012), taste learning (Schier et al, 2016; Kayyal et al, 2021; Yiannakas et al, 2021; Arieli et al, 2022) and expectation (Samuelsen et al, 2012; Gardner and Fontanini, 2014; Vincis and Fontanini, 2016; Livneh et al, 2017), but also in taste-based decision making (Mukherjee et al, 2019; Vincis et al, 2020), highlighting its role not only in sensory processing, but also in modulating consummatory behaviors. Therefore, encoding oral thermal signals by the GC could help improve the fidelity of food evaluation processes, integrating temperature as a crucial parameter in evaluating food quality and palatability (Zellner et al, 1988; Moskowitz, 1973; Torregrossa et al, 2012).…”