Department of Neuroscience, Yale School of Medicine, New Haven, Connecticut 06510, and.
Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403.
J Neurosci. 2019 Dec 11;39(50):10044-10059. doi: 10.1523/JNEUROSCI.1226-18.2019. Epub 2019 Oct 31.
Variability in cortical neuronal responses to sensory stimuli and in perceptual decision making performance is substantial. Moment-to-moment fluctuations in waking state or arousal can account for much of this variability. Yet, this variability is rarely characterized across the full spectrum of waking states, leaving the characteristics of the optimal state for sensory processing unresolved. Using pupillometry in concert with extracellular multiunit and intracellular whole-cell recordings, we found that the magnitude and reliability of visually evoked responses in primary visual cortex (V1) of awake, passively behaving male mice increase as a function of arousal and are largest during sustained locomotion periods. During these high-arousal, sustained locomotion periods, cortical neuronal membrane potential was at its most depolarized and least variable. Contrastingly, behavioral performance of mice on two distinct visual detection tasks was generally best at a range of intermediate arousal levels, but worst during high arousal with locomotion. These results suggest that large, reliable responses to visual stimuli in V1 occur at a distinct arousal level from that associated with optimal visual detection performance. Our results clarify the relation between neuronal responsiveness and the continuum of waking states, and suggest new complexities in the relation between primary sensory cortical activity and behavior. Cortical sensory processing strongly depends on arousal. In the mouse visual system, locomotion (associated with high arousal) has previously been shown to enhance the sensory responses of neurons in primary visual cortex (V1). Yet, arousal fluctuates on a moment-to-moment basis, even during quiescent periods. The characteristics of V1 sensory processing across the continuum of arousal are unclear. Furthermore, the arousal level corresponding to optimal visual detection performance is unknown. We show that the magnitude and reliability of sensory-evoked V1 responses are monotonic increasing functions of arousal, and largest during locomotion. Visual detection behavior, however, is suboptimal during high arousal with locomotion, and usually best during intermediate arousal. Our study provides a more complete picture of the dependence of V1 sensory processing on arousal.
皮质神经元对感觉刺激的反应以及知觉决策表现的可变性很大。清醒状态或觉醒时的瞬间波动可以解释其中的大部分可变性。然而，这种可变性很少在整个清醒状态谱中得到描述，使得感觉处理的最佳状态的特征仍未解决。我们使用瞳孔测量法与细胞外多单位和细胞内全细胞记录相结合，发现雄性小鼠清醒时被动行为的初级视觉皮层 (V1) 中视觉诱发电响应的幅度和可靠性随觉醒程度增加，在持续运动期间最大。在这些高唤醒、持续运动期间，皮质神经元膜电位最为去极化且变化最小。相反，在两个不同的视觉检测任务中，老鼠的行为表现通常在中等觉醒水平范围内最佳，但在高唤醒伴有运动时最差。这些结果表明，V1 对视觉刺激的大而可靠的反应发生在与最佳视觉检测性能相关的特定觉醒水平。我们的结果阐明了神经元反应性与清醒状态连续体之间的关系，并表明了初级感觉皮质活动与行为之间关系的新复杂性。皮质感觉处理强烈依赖于觉醒。在小鼠视觉系统中，运动（与高觉醒相关）先前已被证明可以增强初级视觉皮层 (V1) 神经元的感觉反应。然而，即使在静止期间，觉醒也会瞬间波动。在整个觉醒连续体中 V1 感觉处理的特征尚不清楚。此外，最佳视觉检测性能对应的觉醒水平尚不清楚。我们表明，感觉诱发 V1 反应的幅度和可靠性是觉醒的单调递增函数，在运动期间最大。然而，在高唤醒伴有运动时，视觉检测行为不佳，而在中等唤醒时通常最佳。我们的研究提供了 V1 感觉处理对觉醒依赖性的更完整描述。
