Parallel Coding of First- and Second-Order Stimulus Attributes by Midbrain Electrosensory Neurons
Parallel Coding of First- and Second-Order Stimulus Attributes by Midbrain Electrosensory Neurons
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DOI：
10.1523/jneurosci.0478-12.2012
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发表时间：
2012-04-18
影响因子：
5.3
通讯作者：
Chacron, Maurice J.
中科院分区：
文献类型：
--
作者：
McGillivray, Patrick;Vonderschen, Katrin;Chacron, Maurice J.
自然刺激通常具有时变的一阶（即平均值）和二阶（即方差）属性，每个属性都携带感知的关键信息，并且可以在数量级上独立变化。实验表明，感觉系统根据这些属性的变化不断调整其反应。这种适应在神经代码中产生了模糊性，因为多种刺激可能会引发相同的神经反应。虽然通过单独的神经通路对一阶和二阶属性进行并行处理足以消除这种模糊性，但迄今为止尚未发现此类通路的存在以及介导其出现的神经回路。我们记录了弱电鱼 Apteronotus leptorhynchus 的中脑电感觉神经元对具有随时间独立变化的一阶和二阶属性的刺激的反应。我们发现了三组不同的中脑神经元：第一组对一阶属性和二阶属性都有反应，第二组选择性地响应一阶属性，最后一组选择性地响应二阶属性。相比之下，所有传入后脑神经元都对一阶和二阶属性做出反应。通过计算分析，我们展示了如何将来自开型和关型传入神经元的异质群体的输入组合起来，从而对中脑神经元中的一阶或二阶刺激属性产生反应选择性。因此，我们的研究首次揭示了大脑中出现一阶和二阶刺激属性的并行处理的通用且广泛适用的机制。
Natural stimuli often have time-varying first-order (i.e., mean) and second-order (i.e., variance) attributes that each carry critical information for perception and can vary independently over orders of magnitude. Experiments have shown that sensory systems continuously adapt their responses based on changes in each of these attributes. This adaptation creates ambiguity in the neural code as multiple stimuli may elicit the same neural response. While parallel processing of first-and second-order attributes by separate neural pathways is sufficient to remove this ambiguity, the existence of such pathways and the neural circuits that mediate their emergence have not been uncovered to date. We recorded the responses of midbrain electrosensory neurons in the weakly electric fish Apteronotus leptorhynchus to stimuli with first-and second-order attributes that varied independently in time. We found three distinct groups of midbrain neurons: the first group responded to both first-and second-order attributes, the second group responded selectively to first-order attributes, and the last group responded selectively to second-order attributes. In contrast, all afferent hindbrain neurons responded to both first-and second-order attributes. Using computational analyses, we show how inputs from a heterogeneous population of ON-and OFF-type afferent neurons are combined to give rise to response selectivity to either first-or second-order stimulus attributes in midbrain neurons. Our study thus uncovers, for the first time, generic and widely applicable mechanisms by which parallel processing of first-and second-order stimulus attributes emerges in the brain.