Adult-neurogenesis allows for representational stability and flexibility in early olfactory system

In the early olfactory system, adult-neurogenesis, a process of neuronal replacement results in the continuous reorganization of synaptic connections and network architecture throughout the animal’s life. This poses a critical challenge: How does the olfactory system maintain stable representations of odors and therefore allow for stable sensory perceptions amidst this ongoing circuit instability? Utilizing a detailed spiking network model of early olfactory circuits, we uncovered dual roles for adult-neurogenesis: one that both supports representational stability to faithfully encode odor information and also one that facilitates plasticity to allow for learning and adaptation. In the main olfactory bulb, adult-neurogenesis affects neural codes in individual mitral and tufted cells but preserves odor representations at the neuronal population level. By contrast, in the olfactory piriform cortex, both individual cell responses and overall population dynamics undergo progressive changes due to adult-neurogenesis. This leads to representational drift, a gradual alteration in sensory perception. Both processes are dynamic and depend on experience such that repeated exposure to specific odors reduces the drift due to adult-neurogenesis; thus, when the odor environment is stable over the course of adult-neurogenesis, it is neurogenesis that actually allows the representations to remain stable in piriform cortex; when those olfactory environments change, adult-neurogenesis allows the cortical representations to track environmental change. Whereas perceptual stability and plasticity due to learning are often thought of as two distinct, often contradictory processing in neuronal coding, we find that adult-neurogenesis serves as a shared mechanism for both. In this regard, the quixotic presence of adult-neurogenesis in the mammalian olfactory bulb that has been the focus of considerable debate in chemosensory neuroscience may be the mechanistic underpinning behind an array of complex computations.

在早期嗅觉系统中，成年神经发生这一神经元替换过程导致在动物的整个生命周期中突触连接和网络结构不断重组。这带来了一个关键挑战：在这种持续的电路不稳定情况下，嗅觉系统如何保持气味的稳定表征，从而实现稳定的感官知觉呢？利用一个详细的早期嗅觉电路的脉冲网络模型，我们揭示了成年神经发生的双重作用：一种作用是支持表征稳定性以忠实地编码气味信息，另一种作用是促进可塑性以实现学习和适应。在主嗅球中，成年神经发生影响单个 mitral细胞和tufted细胞的神经编码，但在神经元群体水平上保留气味表征。相比之下，在梨状皮质中，由于成年神经发生，单个细胞的反应和整体群体动态都经历渐进性变化。这导致表征漂移，即感官知觉的逐渐改变。这两个过程都是动态的，并且依赖于经验，例如反复接触特定气味会减少由于成年神经发生导致的漂移；因此，当气味环境在成年神经发生过程中稳定时，实际上是神经发生使得梨状皮质中的表征保持稳定；当那些嗅觉环境改变时，成年神经发生使得皮质表征能够追踪环境变化。虽然由于学习导致的知觉稳定性和可塑性在神经元编码中常常被视为两种不同的、往往相互矛盾的过程，但我们发现成年神经发生是两者的共同机制。在这方面，哺乳动物嗅球中成年神经发生的奇特存在一直是化学感觉神经科学中大量争论的焦点，它可能是一系列复杂计算背后的机制基础。