Plasticity in olfactory bulb circuits
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.
References (55)
- et al.
Visualizing an olfactory sensory map
Cell
(1996) - et al.
Dynamic sensory representations in the olfactory bulb: modulation by wakefulness and experience
Neuron
(2012) - et al.
Odor processing by adult-born neurons
Neuron
(2014) - et al.
Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales
Neuron
(2008) - et al.
Balancing the robustness and efficiency of odor representations during learning
Neuron
(2016) - et al.
Active sampling state dynamically enhances olfactory bulb odor representation
Neuron
(2018) - et al.
Rapid task-dependent tuning of the mouse olfactory bulb
eLife
(2019) - et al.
The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase
Brain Res Bull
(1984) - et al.
Long-term plasticity of excitatory inputs to granule cells in the rat olfactory bulb
Nat Neurosci
(2009) - et al.
Action of the noradrenergic system on adult-born cells is required for olfactory learning in mice
J Neurosci
(2012)
Developmental broadening of inhibitory sensory maps
Nat Neurosci
The association between olfaction and depression: a systematic review
Chem Senses
Rapid and continuous activity-dependent plasticity of olfactory sensory input
Nat Commun
Fear learning enhances neural responses to threat-predictive sensory stimuli
Science
Extinction reverses olfactory fear-conditioned increases in neuron number and glomerular size
Proc Natl Acad Sci U S A
Long term functional plasticity of sensory inputs mediated by olfactory learning
eLife
Lack of Pattern separation in sensory inputs to the olfactory bulb during perceptual learning
eNeuro
Neuronal pattern separation in the olfactory bulb improves odor discrimination learning
Nat Neurosci
A lifetime of neurogenesis in the olfactory system
Front Neurosci
Neuronal organization of olfactory bulb circuits
Front Neural Circuits
Experience-dependent plasticity of mature adult-born neurons
Nat Neurosci
“Silent” mitral cells dominate odor responses in the olfactory bulb of awake mice
Nat Neurosci
Distinct spatiotemporal activity in principal neurons of the mouse olfactory bulb in anesthetized and awake states
Front Neural Circuits
Sparse odor coding in awake behaving mice
J Neurosci
Context- and output layer-dependent long-term ensemble plasticity in a sensory circuit
Neuron
Stimulation of the locus ceruleus modulates signal-to-noise ratio in the olfactory bulb
J Neurosci
Mechanisms of pattern decorrelation by recurrent neuronal circuits
Nat Neurosci
Cited by (15)
BDNF-dependent signaling in the olfactory bulb modulates social recognition memory in mice
2024, Neurobiology of Learning and MemoryA biomimetic sensor using neurotransmitter detection to decode odor perception by an olfactory network
2022, Biosensors and BioelectronicsCitation Excerpt :ORNs send projections to the apical dendrites of mitral and tufted (MT) cells within the olfactory glomeruli of the OB and trigger the release of glutamate at the synapses (Economo et al., 2016). The dendrites of MT cells express ionic and metabotropic glutamate receptors to detect the glutamate released by other cells (Wu et al., 2020). Excitatory patterns of MT cells are further modulated through the activity of GABAergic interneurons such as granule cells and periglomerular (PG) cells, and glutamatergic interneurons such as external tufted (ET) cells (Lage-Rupprecht et al., 2020).
Editorial overview: Systems neuroscience
2020, Current Opinion in NeurobiologyBridging event-related potentials with behavioral studies in motor learning
2023, Frontiers in Integrative Neuroscience
- †
These authors contributed equally and the order was determined by a coin flip.