Experience-dependent evolution of odor mixture representations in piriform cortex

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 mi...

Full description

Bibliographic Details
Main Authors: Alice Berners-Lee, Elizabeth Shtrahman, Julien Grimaud, Venkatesh N. Murthy
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-04-01
Series:PLoS Biology
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10129003/?tool=EBI
_version_ 1797837228368461824
author Alice Berners-Lee
Elizabeth Shtrahman
Julien Grimaud
Venkatesh N. Murthy
author_facet Alice Berners-Lee
Elizabeth Shtrahman
Julien Grimaud
Venkatesh N. Murthy
author_sort Alice Berners-Lee
collection DOAJ
description 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. The neural representation of important features of the environment can change as an animal learns. This study shows that salient odor mixtures become over-represented and distinct in the olfactory cortex of mice, allowing a better and more robust categorization of these stimuli.
first_indexed 2024-04-09T15:22:31Z
format Article
id doaj.art-5ee824b19d424d678a6031eaeece7d88
institution Directory Open Access Journal
issn 1544-9173
1545-7885
language English
last_indexed 2024-04-09T15:22:31Z
publishDate 2023-04-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj.art-5ee824b19d424d678a6031eaeece7d882023-04-29T05:30:52ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-04-01214Experience-dependent evolution of odor mixture representations in piriform cortexAlice Berners-LeeElizabeth ShtrahmanJulien GrimaudVenkatesh N. MurthyRodents 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. The neural representation of important features of the environment can change as an animal learns. This study shows that salient odor mixtures become over-represented and distinct in the olfactory cortex of mice, allowing a better and more robust categorization of these stimuli.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10129003/?tool=EBI
spellingShingle Alice Berners-Lee
Elizabeth Shtrahman
Julien Grimaud
Venkatesh N. Murthy
Experience-dependent evolution of odor mixture representations in piriform cortex
PLoS Biology
title Experience-dependent evolution of odor mixture representations in piriform cortex
title_full Experience-dependent evolution of odor mixture representations in piriform cortex
title_fullStr Experience-dependent evolution of odor mixture representations in piriform cortex
title_full_unstemmed Experience-dependent evolution of odor mixture representations in piriform cortex
title_short Experience-dependent evolution of odor mixture representations in piriform cortex
title_sort experience dependent evolution of odor mixture representations in piriform cortex
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10129003/?tool=EBI
work_keys_str_mv AT alicebernerslee experiencedependentevolutionofodormixturerepresentationsinpiriformcortex
AT elizabethshtrahman experiencedependentevolutionofodormixturerepresentationsinpiriformcortex
AT juliengrimaud experiencedependentevolutionofodormixturerepresentationsinpiriformcortex
AT venkateshnmurthy experiencedependentevolutionofodormixturerepresentationsinpiriformcortex