Werth Jesse C, Einhorn Matthew, Cleland Thomas A
Department of Psychology, Cornell University, Ithaca, New York, United States.
J Neurophysiol. 2025 Jul 1;134(1):274-286. doi: 10.1152/jn.00340.2024. Epub 2025 Jun 14.
In the mammalian olfactory bulb (OB), gamma oscillations in the local field potential are generated endogenously during odor sampling. Such oscillations arise from dynamical systems that generate organized periodic behavior in neural circuits and correspond to spike timing constraints at millisecond timescales. Although the cellular and network mechanisms of gamma oscillogenesis in the OB are reasonably well established, it remains unclear how these fine-timescale dynamics serve to represent odors. Are patterns of spike synchronization on the gamma timescale replicable and odor-specific? Does the transformation to a spike-timing metric embed additional signal processing computations? To address these questions, we used OB slice recordings to examine the spike timing dynamics evoked by "fictive odorants" generated via spatiotemporally patterned optogenetic stimulation of olfactory sensory neuron axonal arbors. We found that a small proportion of mitral/tufted cells phase-lock strongly to the fast oscillations evoked by fictive odorants and exhibit tightly coupled spike-spike synchrony on the gamma timescale. Moreover, the specific population of synchronized neurons corresponded to the "quality," but not the "concentration" (intensity), of the fictive odorant presented, and was conserved across multiple presentations of the same fictive odorant. Given the established selectivity of piriform cortical pyramidal neurons for inputs synchronized on this timescale, we conclude that spike synchronization on a milliseconds timescale is a metric by which the OB encodes and exports afferent odor information in a concentration-invariant manner. As a corollary, mitral/tufted cell spikes that are not organized in time are unlikely to contribute meaningfully to the ensemble odor representation. Neurophysiological activity patterns often are interpreted as simple mean spike rates, without consideration of the intrinsic representational timescales established by the dynamical systems of the brain. We here show that principal neuron spike timing in the olfactory bulb circuit is regulated by such fast internal network dynamics, and that these tightly synchronized spikes encode sensory information into a form interpretable by downstream target neurons.
在哺乳动物的嗅球（OB）中，局部场电位的伽马振荡是在气味采样过程中内源性产生的。这种振荡源于在神经回路中产生有组织的周期性行为的动力系统，并对应于毫秒时间尺度上的尖峰时间约束。尽管OB中伽马振荡产生的细胞和网络机制已得到相当充分的确立，但这些精细时间尺度的动力学如何用于表征气味仍不清楚。伽马时间尺度上的尖峰同步模式是否可复制且具有气味特异性？转换为尖峰时间度量是否嵌入了额外的信号处理计算？为了解决这些问题，我们使用OB切片记录来检查通过对嗅觉感觉神经元轴突 Arbor 进行时空模式光遗传学刺激产生的“虚拟气味剂”所诱发的尖峰时间动态。我们发现，一小部分二尖瓣/簇状细胞与虚拟气味剂诱发的快速振荡强烈锁相，并在伽马时间尺度上表现出紧密耦合的尖峰 - 尖峰同步。此外，同步神经元的特定群体对应于所呈现虚拟气味剂的“质量”，而非“浓度”（强度），并且在同一虚拟气味剂的多次呈现中保持不变。鉴于梨状皮质锥体神经元对在此时间尺度上同步的输入具有既定的选择性，我们得出结论，毫秒时间尺度上的尖峰同步是OB以浓度不变的方式编码和输出传入气味信息的一种度量。作为推论，未及时组织的二尖瓣/簇状细胞尖峰不太可能对整体气味表征有意义地做出贡献。神经生理活动模式通常被解释为简单的平均尖峰率，而不考虑大脑动力系统所确立的内在表征时间尺度。我们在此表明，嗅球回路中主神经元的尖峰时间受此类快速内部网络动力学调节，并且这些紧密同步的尖峰将感官信息编码为下游目标神经元可解释的形式。
