Elsevier

Current Opinion in Neurobiology

Volume 64, October 2020, Pages 17-23
Current Opinion in Neurobiology

Plasticity in olfactory bulb circuits

https://doi.org/10.1016/j.conb.2020.01.007Get rights and content

Highlights

  • Learning induces mitral cell sparsening and pattern decorrelation.

  • GCs mediate lateral inhibition to facilitate pattern separation of mitral cells.

  • Adult-born neurons mediate the plasticity essential for difficult discrimination.

  • Olfactory bulb optimally represents the dynamic olfactory environment.

Olfaction is crucial for animal survival and human well-being. The olfactory bulb is the obligatory input station for olfactory information. In contrast to the traditional view as a static relay station, recent evidence indicates that the olfactory bulb dynamically processes olfactory information in an experience-dependent and context-dependent manner. Here, we review recent studies on experience-dependent plasticity of the main circuit components within the olfactory bulb of rodents. We argue that the olfactory bulb plasticity allows optimal representations of behaviorally-relevant odors in the continuously changing olfactory environment.

Introduction

The ability to navigate a complex olfactory environment adaptively is crucial in various behavioral contexts, such as foraging for food and avoiding predators. Olfaction is particularly crucial for rodents that rely heavily on their sense of smell and accordingly are equipped with a highly evolved olfactory system. Even in humans that are often considered to depend mainly on other senses such as vision, anosmic patients report fear due to their inability to detect a gas leak and identify rotten food and often suffer from depression [1]. The olfactory bulb is the obligatory input station of olfactory information, receiving direct sensory inputs from the nose and transmitting the information to the rest of the brain. The olfactory bulb comprises a relatively simple feedforward pathway, and thus it has been tempting to speculate that the olfactory bulb is a simple relay station while significant information processing occurs in downstream brain centers. This conventional dogma has been, however, challenged by recent findings that showed that the olfactory bulb dynamically processes odorant information in a state-dependent and experience-dependent manner. Moreover, the olfactory bulb is one of the two loci in the rodent brain where new neurons are incorporated every day to the existing circuit throughout life. These adult-born neurons migrate from the subventricular zone in the central brain and differentiate into local inhibitory neurons in the bulb, providing an additional level of plasticity. In this review, we will summarize recent literature on experience-dependent plasticity of the olfactory bulb circuit (Figure 1) in rodents. We propose that the principal function of the olfactory bulb is to optimally represent the behaviorally relevant odorants by continuously updating its circuits based on the ongoing statistical structure of the olfactory environment.

Section snippets

OSN inputs and glomeruli

Odorants are detected by olfactory sensory neurons (OSNs) in the olfactory epithelium inside the nasal cavity, each of which expresses one of ∼1000 odorant receptor genes. OSNs expressing the same odorant receptor extend their axons to two of ∼2000 glomeruli in the glomerular layer of the olfactory bulb [2]. At glomeruli, OSN axons make glutamatergic synapses on the projection neurons (mitral/tufted cells) and local interneurons. Several studies have found that OSN inputs to the bulb show a

Mitral and tufted cells

Mitral cells and tufted cells are the two types of projection neurons in the olfactory bulb located in the mitral cell layer and the external plexiform layer (EPL), respectively. Each mitral/tufted cell projects their single primary apical dendrite to only one glomerulus where they receive inputs from the axons of OSNs expressing the same receptor [11]. Mitral/tufted cells directly project their axons to higher structures in the brain and are the sole source of olfactory information for the

Granule cells

As summarized above, olfactory perceptual learning induces an improved pattern separation of odor representations by mitral cell ensembles. Such a pattern decorrelation is likely mediated by plasticity to generate circuits for selective inhibition that can amplify the difference between similar patterns of mitral cell activity [23]. Granule cells (GCs) are the main source of lateral inhibition in the olfactory bulb, extending dendrites in the EPL and forming reciprocal, dendrodendritic synapses

Concluding remarks

Here, we reviewed the recent advances on plasticity of the rodent olfactory bulb. An emerging view is that the olfactory bulb is not a passive relay station but a dynamic signal processing unit that facilitates the encoding of behaviorally relevant odorants. An intriguing question is why the olfactory bulb evolved to be such a dynamic system that takes advantage of highly plastic adult-born neurons to constantly adjust the way it processes incoming sensory information, a strategy not utilized

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank the members of the Komiyama lab, especially Q. Chen, for the feedback and discussions. This work was supported by grants from N.I.H. (R01 DC014690, R01 NS091010A, R01 EY025349, and P30EY022589), David and Lucile Packard Foundation, and NSF (1734940) to T.K.

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