Value-related learning in the olfactory bulb occurs through pathway-dependent perisomatic inhibition of mitral cells

PLoS Biol. 2024 Mar 1;22(3):e3002536. doi: 10.1371/journal.pbio.3002536. eCollection 2024 Mar.

Abstract

Associating values to environmental cues is a critical aspect of learning from experiences, allowing animals to predict and maximise future rewards. Value-related signals in the brain were once considered a property of higher sensory regions, but their wide distribution across many brain regions is increasingly recognised. Here, we investigate how reward-related signals begin to be incorporated, mechanistically, at the earliest stage of olfactory processing, namely, in the olfactory bulb. In head-fixed mice performing Go/No-Go discrimination of closely related olfactory mixtures, rewarded odours evoke widespread inhibition in one class of output neurons, that is, in mitral cells but not tufted cells. The temporal characteristics of this reward-related inhibition suggest it is odour-driven, but it is also context-dependent since it is absent during pseudo-conditioning and pharmacological silencing of the piriform cortex. Further, the reward-related modulation is present in the somata but not in the apical dendritic tuft of mitral cells, suggesting an involvement of circuit components located deep in the olfactory bulb. Depth-resolved imaging from granule cell dendritic gemmules suggests that granule cells that target mitral cells receive a reward-related extrinsic drive. Thus, our study supports the notion that value-related modulation of olfactory signals is a characteristic of olfactory processing in the primary olfactory area and narrows down the possible underlying mechanisms to deeper circuit components that contact mitral cells perisomatically.

MeSH terms

  • Animals
  • Mice
  • Neurons* / physiology
  • Odorants
  • Olfactory Bulb* / physiology
  • Smell / physiology
  • Synapses / physiology

Grants and funding

This work was supported by Grant-in-Aid for Scientific Research (C) 22K06490 (https://www.jsps.go.jp/english/e-grants/ to SL & IF) and OIST Graduate University (https://www.oist.jp/ to SL, XF, JKR, & IF). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.