The ability to group sensory stimuli into categories is crucial for efficient interaction with a rich and ever-changing environment. In olfaction, basic features of categorical representation of odors were observed as early as in the olfactory bulb (OB). Categorical representation was described in mitral cells (MCs) as sudden transitions in responses to odors that were morphed along a continuum. However, it remains unclear to what extent such response dynamics actually reflect perceptual categories and decisions therein. Here, we tested the role of learning on category formation in the mouse OB, using in vivo two-photon calcium imaging and behavior. We imaged MC responses in naive mice and in awake behaving mice as they learned two tasks with different classification logic. In one task, a one-decision-boundary task, animals learned to classify odor mixtures based on the dominant compound in the mixtures. As expected, categorical representation of odors, which was evident already in naive animals, further increased following learning. In a second task, a multi-decision-boundary task, animals learned to classify odors independent of their chemical similarity. Here, odor discrimination was based on the meaning ascribed to them (either rewarding or not). Following the multi-decision-boundary task, odor representations by MCs reorganized according to the odor value in the new category. This functional reorganization was also reflected as a shift from predominantly excitatory odor responses to predominantly inhibitory odor responses. Our data show that odor representations by MCs are flexible, are shaped by task demands, and carry category-related information.
Bibliographical noteFunding Information:
We thank Israel Nelken for invaluable advice on the behavioral paradigm and analyses. We thank Amit Vinograd, Merav Ahissar, Yoram Ben Shaul, Israel Nelken, and members of the Mizrahi lab for comments on early versions of the manuscript and for discussions. We thank Ariel Gilad for sharing scripts and Merav Givon and Itzik Simchayof for technical assistance. This work was supported by an ERC consolidators grant to A.M. (no. 616063), an Israel Science Foundation grant to A.M. (no. 224/17), and a German Israeli Foundation grant to A.M. (I-1479-418.13/2018). E.K. designed and conducted all main experiments. E.K. and E.M. analyzed the data. E.M. wrote code for population analysis. E.K. built the behavioral apparatus, and D.P. wrote the code for behavioral training and data acquisition. H.S.-N. performed some imaging experiments. A.M. funded and supervised the project. E.K. and A.M. wrote the paper. The authors declare no competing interests.
© 2021 Elsevier Inc.
- calcium imaging
- two photon