Experience-dependent evolution of odor mixture representations in piriform cortex

Abstract

Rodents can learn from exposure to rewarding odors to make better and quicker decisions. The piriform cortex is thought to be important for learning complex odor associations; however, it is not understood exactly how it learns to remember discriminations between many, sometimes overlapping, odor mixtures. We investigated how odor mixtures are represented in the posterior piriform cortex (pPC) of mice while they learn to discriminate a unique target odor mixture against hundreds of nontarget mixtures. We find that a significant proportion of pPC neurons discriminate between the target and all other nontarget odor mixtures. Neurons that prefer the target odor mixture tend to respond with brief increases in firing rate at odor onset compared to other neurons, which exhibit sustained and/or decreased firing. We allowed mice to continue training after they had reached high levels of performance and find that pPC neurons become more selective for target odor mixtures as well as for randomly chosen repeated nontarget odor mixtures that mice did not have to discriminate from other nontargets. These single unit changes during overtraining are accompanied by better categorization decoding at the population level, even though behavioral metrics of mice such as reward rate and latency to respond do not change. However, when difficult ambiguous trial types are introduced, the robustness of the target selectivity is correlated with better performance on the difficult trials. Taken together, these data reveal pPC as a dynamic and robust system that can optimize for both current and possible future task demands at once.

Neural Circuits for Fast Poisson Compressed Sensing in the Olfactory Bulb

“…This computational problem differs from many experimental tasks focusing on discrimination between two odorants [60], which underlie most scientific work on rodent olfactory decision making [60][61][62]. Here, the goal is to identify the components of a complex olfactory scene [63][64][65][66]. Importantly, the limits of human performance in this setting remain to our knowledge unknown [67,68].…”

“…This computational problem differs from many experimental tasks focusing on discrimination between two odorants (Uchida and Mainen, 2003), which underlie most scientific work on rodent olfactory decision making (Uchida and Mainen, 2003;Spors et al, 2012;Reinert and Fukunaga, 2022). Here, the goal is to identify the components of a complex olfactory scene (Rokni et al, 2014;Lebovich et al, 2021;Li et al, 2023;Berners-Lee et al, 2023). To render the problem more tractable, we will make a number of simplifications of the anatomy and physiology of the OB.…”

Effects of stochastic coding on olfactory discrimination in flies and mice

“…What is also evident, however, is that unreliable cells, too, provide significant distinguishing information between any pair of odors. Thus, our analysis of the data using linear (and nonparametric) decoders and statistical analysis shows that discrimination between odors becomes hard when their similarity increases, reflecting experimental findings of difficulties organisms face when discerning similar odors [ 3 , 9 , 71 , 72 ].…”

Olfactory Critical Periods: How Odor Exposure Shapes the Developing Brain in Mice and Flies

“…Experience can shape neuronal circuits at any time during the life of an organism. For example, repeated exposure to the same odor stimulus improves the robustness and discriminability of the odor responses in fruit flies and mice [37][38][39][40][41][42]. However, neuronal circuits are more susceptible to experience-dependent neuronal plasticity during the critical period [43].…”

“…These examples underscore the importance of circuit refinement unique to the chemical environment to which the organism is exposed. For example, repeated exposure to the same odor stimulus improves the robustness of the odor responses and discriminability in fruit flies and mice [37][38][39][40][41][42]. However, despite the importance of the critical period in olfactory plasticity and refinement of circuits, the cellular and molecular mechanisms underlying the olfactory critical period have not been as extensively studied as visual critical periods.…”