Abstract

Both passive exposure and active learning through reinforcement enhance fine sensory discrimination abilities. In the olfactory system, this enhancement is thought to occur partially through the integration of adult-born inhibitory interneurons resulting in a refinement of the representation of overlapping odorants. Here, we identify in mice a novel and unexpected dissociation between passive and active learning at the level of adult-born granule cells. Specifically, while both passive and active learning processes augment neurogenesis, adult-born cells differ in their morphology, functional coupling and thus their impact on olfactory bulb output. Morphological analysis, optogenetic stimulation of adult-born neurons and mitral cell recordings revealed that passive learning induces increased inhibitory action by adult-born neurons, probably resulting in more sparse and thus less overlapping odor representations. Conversely, after active learning inhibitory action is found to be diminished due to reduced connectivity. In this case, strengthened odor response might underlie enhanced discriminability.

Highlights

  • Brain representations of the environment constantly evolve through learning mediated by different plasticity mechanisms

  • We found that implicit learning decreased the number of odor-activated M/T cells compared to non-enriched controls (587 ± 29 M/T cells counted per animal; Enr, n = 5 and Non-Enr, n = 4; Bonferroni-corrected test p=0.02; Table 1, Figure 1J and Figure 1—source data 1), resulting in a sparser representation of learned odorants at the olfactory bulb (OB) output

  • While the number of integrated adult-born granule cells was similar in both forms of learning, they differed in the synaptic integration mode of adult-born neurons and their effect on M/T cell responses to odor

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Summary

Introduction

Brain representations of the environment constantly evolve through learning mediated by different plasticity mechanisms. Both passive (implicit perceptual learning in response to repeated exposure) and active (explicit associative learning in response to reinforcement) learning can improve discrimination between similar odorants (Mandairon et al, 2006a; Moreno et al, 2009). Both forms of learning have been shown to modulate neural activity in the OB (Buonviso et al, 1998; Kay and Laurent, 1999; Doucette et al, 2011), and to increase survival of inhibitory adult-born interneurons

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