Diverse processing underlying frequency integration in midbrain neurons of barn owls.

Diverse processing underlying frequency integration in midbrain neurons of barn owls.
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DOI:
10.1371/journal.pcbi.1009569
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发表时间:
2021-11
影响因子:
4.3
通讯作者:
Fischer BJ
Fischer BJ
中科院分区:
生物学2区
文献类型:
--
作者:
Gorman JC;Tufte OL;Miller AVR;DeBello WM;Peña JL;Fischer BJ

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感觉神经元的涌现反应特性取决于电路连接性和体树处理。仓鸮下丘外核(ICx)的神经元显示空间选择性的出现。这些神经元使用耳间时间差(ITD)作为声源水平方向的提示。ITD由具有窄频率调谐的上游脑干神经元检测,导致空间模糊的响应。这种空间模糊性是通过ICx神经元在频率上整合输入来解决的,这是跨物种声音定位的相关处理。以前的模型预测ICx神经元作为点神经元,在频率上线性积分输入。然而,ICx神经元复杂的树突树和棘提出了这种预测是否准确的问题。来自ICx神经元的体内细胞内记录的数据被用来解决这个问题。结果显示不同的频率整合特性,其中一些ICx神经元表现出与点神经元假设和其他非线性树突整合一致的反应。模型表明,不同的连接模式和形式的树突处理可能是所观察到的ICx神经元的频率整合处理的基础。这些结果证实了神经元与复杂的树突树实现不同的线性和非线性整合的突触输入,自适应编码和学习的相关性,并支持在声音定位的基本机制的能力。在感觉通路的更高阶段的神经元通常显示出对感觉刺激的特性的选择性,这些特性是由神经系统内执行的计算产生的。这些紧急反应特性可以由单个细胞内发生的神经连接和处理模式产生。在这里,我们调查是否神经连接和单神经元计算可能有助于仓鸮的中脑听觉神经元的空间选择性的出现。我们使用来自体内细胞内记录的数据来测试来自先前建模工作的假设,即这些细胞作为点神经元在其阈下响应中执行其输入的线性和。结果表明,虽然一些神经元的反应与点神经元的假设一致,其他匹配的非线性集成的预测,表明跨神经元的频率集成特性的多样性。建模进一步表明,不同的连接模式和单神经元计算形式可能是观察到的反应的基础。这些结果表明,具有复杂形态的神经元可以实现与自适应编码和学习相关的突触输入的多样化整合。
Emergent response properties of sensory neurons depend on circuit connectivity and somatodendritic processing. Neurons of the barn owl’s external nucleus of the inferior colliculus (ICx) display emergence of spatial selectivity. These neurons use interaural time difference (ITD) as a cue for the horizontal direction of sound sources. ITD is detected by upstream brainstem neurons with narrow frequency tuning, resulting in spatially ambiguous responses. This spatial ambiguity is resolved by ICx neurons integrating inputs over frequency, a relevant processing in sound localization across species. Previous models have predicted that ICx neurons function as point neurons that linearly integrate inputs across frequency. However, the complex dendritic trees and spines of ICx neurons raises the question of whether this prediction is accurate. Data from in vivo intracellular recordings of ICx neurons were used to address this question. Results revealed diverse frequency integration properties, where some ICx neurons showed responses consistent with the point neuron hypothesis and others with nonlinear dendritic integration. Modeling showed that varied connectivity patterns and forms of dendritic processing may underlie observed ICx neurons’ frequency integration processing. These results corroborate the ability of neurons with complex dendritic trees to implement diverse linear and nonlinear integration of synaptic inputs, of relevance for adaptive coding and learning, and supporting a fundamental mechanism in sound localization. Neurons at higher stages of sensory pathways often display selectivity for properties of sensory stimuli that result from computations performed within the nervous system. These emergent response properties can be produced by patterns of neural connectivity and processing that occur within individual cells. Here we investigated whether neural connectivity and single-neuron computation may contribute to the emergence of spatial selectivity in auditory neurons in the barn owl’s midbrain. We used data from in vivo intracellular recordings to test the hypothesis from previous modeling work that these cells function as point neurons that perform a linear sum of their inputs in their subthreshold responses. Results indicate that while some neurons show responses consistent with the point neuron hypothesis, others match predictions of nonlinear integration, indicating a diversity of frequency integration properties across neurons. Modeling further showed that varied connectivity patterns and forms of single-neuron computation may underlie observed responses. These results demonstrate that neurons with complex morphologies may implement diverse integration of synaptic inputs, relevant for adaptive coding and learning.
DOI: 10.1038/71125
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影响因子: 25
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