Zavatone-Veth Jacob A, Masset Paul, Tong William L, Zak Joseph D, Murthy Venkatesh N, Pehlevan Cengiz
Center for Brain Science, Harvard University, Cambridge, MA 02138.
Department of Physics, Harvard University, Cambridge, MA 02138.
Adv Neural Inf Process Syst. 2023;36:64793-64828.
Within a single sniff, the mammalian olfactory system can decode the identity and concentration of odorants wafted on turbulent plumes of air. Yet, it must do so given access only to the noisy, dimensionally-reduced representation of the odor world provided by olfactory receptor neurons. As a result, the olfactory system must solve a compressed sensing problem, relying on the fact that only a handful of the millions of possible odorants are present in a given scene. Inspired by this principle, past works have proposed normative compressed sensing models for olfactory decoding. However, these models have not captured the unique anatomy and physiology of the olfactory bulb, nor have they shown that sensing can be achieved within the 100-millisecond timescale of a single sniff. Here, we propose a rate-based Poisson compressed sensing circuit model for the olfactory bulb. This model maps onto the neuron classes of the olfactory bulb, and recapitulates salient features of their connectivity and physiology. For circuit sizes comparable to the human olfactory bulb, we show that this model can accurately detect tens of odors within the timescale of a single sniff. We also show that this model can perform Bayesian posterior sampling for accurate uncertainty estimation. Fast inference is possible only if the geometry of the neural code is chosen to match receptor properties, yielding a distributed neural code that is not axis-aligned to individual odor identities. Our results illustrate how normative modeling can help us map function onto specific neural circuits to generate new hypotheses.
在一次吸气过程中,哺乳动物的嗅觉系统就能解码随紊乱气流飘来的气味分子的身份和浓度。然而,它必须仅通过嗅觉受体神经元提供的气味世界的嘈杂、维度缩减的表征来做到这一点。因此,嗅觉系统必须解决一个压缩感知问题,这依赖于在给定场景中仅存在数百万种可能气味分子中的少数几种这一事实。受此原理启发,过去的研究提出了用于嗅觉解码的规范压缩感知模型。然而,这些模型既没有捕捉到嗅球独特的解剖结构和生理学特性,也没有表明在一次吸气的100毫秒时间尺度内就能实现感知。在这里,我们提出了一种基于速率的泊松压缩感知电路模型来模拟嗅球。该模型映射到嗅球的神经元类别上,并概括了它们连接性和生理学的显著特征。对于与人类嗅球大小相当的电路规模,我们表明该模型能够在一次吸气的时间尺度内准确检测出数十种气味。我们还表明,该模型可以进行贝叶斯后验采样以进行准确的不确定性估计。只有当神经编码的几何结构被选择为与受体特性相匹配时,快速推理才有可能,从而产生一种与单个气味身份不对齐的分布式神经编码。我们的结果说明了规范建模如何帮助我们将功能映射到特定的神经回路以产生新的假设。