Mahoney Institute for Neurosciences, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104.
Mahoney Institute for Neurosciences, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104
J Neurosci. 2018 Jan 17;38(3):595-612. doi: 10.1523/JNEUROSCI.2099-17.2017. Epub 2017 Dec 1.
Inhibition in thalamorecipient layer 4 simple cells of primary visual cortex is believed to play important roles in establishing visual response properties and integrating visual inputs across their receptive fields (RFs). Simple cell RFs are characterized by nonoverlapping, spatially restricted subregions in which visual stimuli can either increase or decrease the firing rate of the cell, depending on contrast. Inhibition is believed to be triggered exclusively from visual stimulation of individual RF subregions. However, this view is at odds with the known anatomy of layer 4 interneurons in visual cortex and differs from recent findings in mouse visual cortex. Here we show with intracellular recordings in cats that while excitation is restricted to RF subregions, inhibition spans the width of simple cell RFs. Consequently, excitatory stimuli within a subregion concomitantly drive excitation and inhibition. Furthermore, we found that the distribution of inhibition across the RF is stronger toward OFF subregions. This inhibitory OFF-subregion bias has a functional consequence on spatial integration of inputs across the RF. A model based on the known anatomy of layer 4 demonstrates that the known proportion and connectivity of inhibitory neurons in layer 4 of primary visual cortex is sufficient to explain broad inhibition with an OFF-subregion bias while generating a variety of phase relations, including antiphase, between excitation and inhibition in response to drifting gratings. The wiring of excitatory and inhibitory neurons in cortical circuits is key to determining the response properties in sensory cortex. In the visual cortex, the first cells that receive visual input are simple cells in layer 4. The underlying circuitry responsible for the response properties of simple cells is not yet known. In this study, we challenge a long-held view concerning the pattern of inhibitory input and provide results that agree with current known anatomy. We show here that inhibition is evoked broadly across the receptive fields of simple cells, and we identify a surprising bias in inhibition within the receptive field. Our findings represent a step toward a unified view of inhibition across different species and sensory systems.
在初级视觉皮层的丘脑接受层 4 简单细胞中，抑制作用被认为在建立视觉反应特性和整合其感受野 (RF) 内的视觉输入方面发挥着重要作用。简单细胞 RF 的特征是不重叠的、空间上受限的子区域，在这些子区域中，视觉刺激可以根据对比度增加或减少细胞的放电率。抑制作用被认为是由单个 RF 子区域的视觉刺激引发的。然而，这种观点与视觉皮层中第 4 层中间神经元的已知解剖结构不一致，也与最近在小鼠视觉皮层中的发现不同。在这里，我们通过猫的细胞内记录表明，虽然兴奋仅限于 RF 子区域，但抑制作用跨越简单细胞 RF 的宽度。因此，子区域内的兴奋刺激同时驱动兴奋和抑制。此外，我们发现抑制作用在 RF 上的分布对 OFF 子区域更强。这种抑制性 OFF 子区域偏差对 RF 上输入的空间整合具有功能影响。基于第 4 层已知解剖结构的模型表明，初级视觉皮层第 4 层中已知比例和连接性的抑制性神经元足以解释具有 OFF 子区域偏差的广泛抑制作用，同时在响应漂移光栅时产生各种相位关系，包括反相。皮质电路中兴奋性和抑制性神经元的连接对于确定感觉皮层中的反应特性至关重要。在视觉皮层中，首先接收视觉输入的细胞是第 4 层的简单细胞。负责简单细胞反应特性的基础电路尚不清楚。在这项研究中，我们对抑制性输入的模式提出了长期以来的观点，并提供了与当前已知解剖结构一致的结果。我们在这里表明，抑制作用广泛地在简单细胞的感受野中被激发，并且我们在感受野中发现了抑制作用的惊人偏差。我们的发现代表了在不同物种和感觉系统中对抑制作用进行统一观点的一个步骤。
