Understanding how heterogeneous neural populations represent sensory input to give rise to behavior remains a central problem in systems neuroscience. Here we investigated how midbrain neurons within the electrosensory system of Apteronotus leptorhynchus code for object location in space. In vivo simultaneous recordings were achieved via Neuropixels probes, high-density electrode arrays, with the stimulus positioned at different locations relative to the animal. Midbrain neurons exhibited heterogeneous response profiles, with a significant proportion (65%) seemingly non-responsive to moving stimuli. Remarkably, we found that non-responsive neurons increased population coding of object location through synergistic interactions with responsive neurons by effectively reducing noise. Mathematical modeling demonstrated that increased response heterogeneity together with the experimentally observed correlations was sufficient to give rise to independent encoding by responsive neurons. Further, addition of non-responsive neurons in the model gave rise to synergistic population coding. Taken together, our findings reveal that non-responsive neurons, which are frequently excluded from analysis, can significantly improve population coding of object location through synergistic interactions with responsive neurons. Combinations of responsive and non-responsive neurons have been observed in sensory systems across taxa; it is likely that similar synergistic interactions improve population coding across modalities and behavioral tasks.Significance Statement Here we show that including the activities of non-responsive neurons with those of responsive neurons increases Fisher information about stimulus location. Further analysis revealed that this is because including non-responsive neurons led to reduced noise levels for responsive neurons. A combination of multi-unit recordings from neural populations and mathematical modeling reveals that response heterogeneity and spatially decaying correlations are necessary to observe this effect. It is likely that synergistic population coding by responsive and non-responsive neurons will be observed in other systems.

中文翻译：

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无响应的神经元改善了物体位置的种群编码。


了解异质神经群如何代表感觉输入以产生行为仍然是系统神经科学的一个核心问题。在这里，我们研究了 Apteronotus leptorhynchus 的电感觉系统内的中脑神经元如何编码空间中的物体位置。通过 Neuropixels 探针、高密度电极阵列实现体内同步记录，刺激位于相对于动物的不同位置。中脑神经元表现出异质性的反应特征，其中很大一部分 （65%） 似乎对移动刺激没有反应。值得注意的是，我们发现无反应神经元通过与响应性神经元的协同相互作用，通过有效降低噪声来增加对象位置的种群编码。数学模型表明，增加的响应异质性以及实验观察到的相关性足以引起响应性神经元的独立编码。此外，在模型中添加无反应的神经元引起了协同群体编码。综上所述，我们的研究结果表明，经常被排除在分析之外的非反应性神经元可以通过与反应性神经元的协同相互作用来显着改善对象位置的种群编码。在各个分类群的感觉系统中观察到反应性和非反应性神经元的组合;类似的协同互动可能会改善跨模式和行为任务的种群编码。意义陈述 在这里，我们表明，将无反应神经元的活动与反应性神经元的活动包括在内会增加有关刺激位置的 Fisher 信息。 进一步的分析表明，这是因为包括无反应的神经元会导致反应性神经元的噪声水平降低。来自神经群体的多单元记录和数学建模的结合表明，响应异质性和空间衰减相关性是观察这种效应所必需的。很可能在其他系统中观察到响应性和非响应性神经元的协同群体编码。