A novel channel of information transmission in the brain: correlations between the activities of medullary neurons encode behaviorally relevant stimuli in weakly electric fish

我们几乎在日常生活的每一个方面都依赖于我们的感官，但我们对大脑如何处理感官刺激以产生可靠行为的了解非常有限。由于单个神经元的活动通常表现出很大的变异性，因此健壮的行为反应的产生被认为是通过结合神经群体的活动(即群体编码)来实现的。为了研究群体编码，科学家们同时记录了许多神经元，这表明神经元的活动往往是相关的，无论是在它们对刺激的平均反应(即信号相关性)方面，还是在它们的变异性(即噪声相关性)方面。虽然人们普遍认为相关性会影响编码，但它们是有益的还是有害的，仍然是科学界激烈辩论的焦点。由于相关性不是固定的，而是根据感觉和行为背景或大脑的内部状态而变化，因此理解相关活动如何影响编码变得更加复杂。然而，这种可塑性允许一个有趣的假设，即相关性本身可以传达关于感觉输入的信息，并在大脑中构成一个独立于单个神经元属性(如放电率)工作的额外信息传输通道。然而，直到今天，这一理论仍未在实验上得到检验。在我的研究期间，我将在弱电鱼类Apteronotus Leptorhynchus的电感觉系统中测试这一假设，Apteronotus Leptorhynchus是一种南美裸体动物，它通过主动产生并持续围绕其身体的电场导航和交流。众所周知，延髓内的电感觉神经元表现出很强的相关性。根据我的初步数据，我假设噪音相关性逐渐编码与行为相关的刺激属性，从而在大脑中提供一个额外的信息传输渠道。在彻底描述完之后，我将阐明使这种新的编码机制成为可能的神经回路的本质。先前的工作表明，许多科学突破是通过对神经系统相对简单和描述良好的模型动物进行研究而实现的，自然刺激的特征也很好，这些都适用于无尾无尾轮虫。此外，这种神经系统的功能原理和分子机制与包括人类在内的高等脊椎动物的神经系统相似。因此，我预计我的发现将对其他模型系统和大脑区域具有广泛的适用性，并将有助于理解相关活动如何影响人口编码。

We rely on our senses in almost every aspect of our everyday live, yet our understanding of how the brain processes sensory stimuli in order to generate reliable behavior is very limited. As the activity of the single neuron typically displays substantial variability, the generation of robust behavioral responses is thought to be achieved by combining the activities of neural populations (i.e. population coding). To investigate population coding, scientists have recorded from many neurons simultaneously which revealed that the activities of neurons are often correlated, both in terms of their average response to a stimulus (i.e. signal correlations) as well in terms of their variabilities (i.e. noise correlations). While it is generally agreed that correlations impact coding, whether they are beneficial or detrimental is still focus of intense debates within the scientific community. Understanding how correlated activity affects coding is furthermore complicated by the fact that correlations are not fixed but change depending on sensory and behavioral context or the internal state of the brain. This plasticity however allows for the interesting hypothesis that correlations themselves could convey information about sensory input and constitute an additional channel of information transmission in the brain that works independent of single neuron attributes (e.g. firing rate). However, to this day this theory remains experimentally untested. During my research fellowship, I will test this hypothesis in the electrosensory system of the weakly electric fish Apteronotus leptorhynchus, a South-American Gymnotid species that navigates and communicates by means of an electric field that is actively generated and constantly surrounds its body. Electrosensory neurons within the medulla are known to display strong correlations. Based on my preliminary data, I hypothesize that noise correlations gradually encode behaviorally relevant stimulus attributes and thus providing an additional channel of information transmission in the brain. After a thorough characterization, I will then elucidate the nature of the neural circuits that enable this novel coding mechanism.Previous work has shown that many scientific breakthroughs were achieved by working on model animals with a relatively simple and well described nervous system and well-characterized natural stimuli, which all apply to Apteronotus leptorhynchus. Furthermore, the functional principles and molecular machinery of this nervous system are similar to those found in higher vertebrates including humans. Consequently, I expect that my findings will have a broad applicability to other model systems and brain areas and will be transformative towards understanding of how correlated activity impacts population coding.