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小鼠初级听觉皮层 L2/3 中具有复杂丘脑皮层和皮层内起源的感受野多样性和旁带抑制。

Diversity of Receptive Fields and Sideband Inhibition with Complex Thalamocortical and Intracortical Origin in L2/3 of Mouse Primary Auditory Cortex.

机构信息

Department of Biology, University of Maryland, College Park, Maryland 20742.

Department of Biomedical Engineering, Johns Hopkins University, Baltimore, Maryland 21205

出版信息

J Neurosci. 2021 Apr 7;41(14):3142-3162. doi: 10.1523/JNEUROSCI.1732-20.2021. Epub 2021 Feb 16.

Abstract

Receptive fields of primary auditory cortex (A1) neurons show excitatory neuronal frequency preference and diverse inhibitory sidebands. While the frequency preferences of excitatory neurons in local A1 areas can be heterogeneous, those of inhibitory neurons are more homogeneous. To date, the diversity and the origin of inhibitory sidebands in local neuronal populations and the relation between local cellular frequency preference and inhibitory sidebands are unknown. To reveal both excitatory and inhibitory subfields, we presented two-tone and pure tone stimuli while imaging excitatory neurons (Thy1) and two types of inhibitory neurons (parvalbumin and somatostatin) in L2/3 of mice A1. We classified neurons into six classes based on frequency response area (FRA) shapes and sideband inhibition depended both on FRA shapes and cell types. Sideband inhibition showed higher local heterogeneity than frequency tuning, suggesting that sideband inhibition originates from diverse sources of local and distant neurons. Two-tone interactions depended on neuron subclasses with excitatory neurons showing the most nonlinearity. Onset and offset neurons showed dissimilar spectral integration, suggesting differing circuits processing sound onset and offset. These results suggest that excitatory neurons integrate complex and nonuniform inhibitory input. Thalamocortical terminals also exhibited sideband inhibition, but with different properties from those of cortical neurons. Thus, some components of sideband inhibition are inherited from thalamocortical inputs and are further modified by converging intracortical circuits. The combined heterogeneity of frequency tuning and diverse sideband inhibition facilitates complex spectral shape encoding and allows for rapid and extensive plasticity. Sensory systems recognize and differentiate between different stimuli through selectivity for different features. Sideband inhibition serves as an important mechanism to sharpen stimulus selectivity, but its cortical mechanisms are not entirely resolved. We imaged pyramidal neurons and two common classes of interneurons suggested to mediate sideband inhibition (parvalbumin and somatostatin positive) in the auditory cortex and inferred their inhibitory sidebands. We observed a higher degree of variability in the inhibitory sideband than in the local frequency tuning, which cannot be predicted from the relative high homogeneity of responses by inhibitory interneurons. This suggests that cortical sideband inhibition is nonuniform and likely results from a complex interplay between existing functional inhibition in the feedforward input and cortical refinement.

摘要

初级听觉皮层 (A1) 神经元的感受野表现出兴奋性神经元的频率偏好和多种抑制侧带。虽然局部 A1 区域的兴奋性神经元的频率偏好可能存在异质性,但抑制性神经元的频率偏好则更为同质。迄今为止,局部神经元群体中抑制侧带的多样性及其起源,以及局部细胞频率偏好与抑制侧带之间的关系尚不清楚。为了揭示兴奋性和抑制性亚区,我们在成像 A1 的 L2/3 中的兴奋性神经元 (Thy1) 和两种类型的抑制性神经元 (parvalbumin 和 somatostatin) 时,呈现了双音和纯音刺激。我们根据频率反应区 (FRA) 形状将神经元分为六类,并根据 FRA 形状和细胞类型对侧带抑制进行分类。侧带抑制的局部异质性高于频率调谐,表明侧带抑制源自局部和远距离神经元的多种来源。双音相互作用取决于神经元亚类,其中兴奋性神经元表现出最强的非线性。起始和结束神经元表现出不同的光谱整合,表明处理声音起始和结束的电路不同。这些结果表明,兴奋性神经元整合复杂且不均匀的抑制性输入。丘脑皮质末梢也表现出侧带抑制,但与皮质神经元的性质不同。因此,侧带抑制的某些成分是从丘脑皮质输入中继承的,并进一步由会聚的皮质内电路进行修饰。频率调谐的组合异质性和多种侧带抑制促进了复杂的光谱形状编码,并允许快速和广泛的可塑性。感觉系统通过对不同特征的选择性来识别和区分不同的刺激。侧带抑制是一种重要的机制,可以锐化刺激选择性,但它的皮质机制尚未完全解决。我们在听觉皮层中对锥体神经元和两种被认为介导侧带抑制的常见中间神经元类 (parvalbumin 和 somatostatin 阳性) 进行了成像,并推断了它们的抑制侧带。我们观察到抑制侧带的可变性比局部频率调谐更高,这不能从抑制性中间神经元的相对高同质性反应中预测。这表明皮质侧带抑制是非均匀的,可能是由于前馈输入中现有功能抑制与皮质细化之间的复杂相互作用所致。

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