School of Life Sciences, University of Sussex, Brighton BN1 9QG, United Kingdom.
Institute of Ophthalmology, University College London, London WC1E 6BT, United Kingdom.
J Neurosci. 2023 Dec 13;43(50):8663-8680. doi: 10.1523/JNEUROSCI.0089-23.2023.
The processing of sensory input is constantly adapting to behavioral demands and internal states. The drive to obtain reward, e.g., searching for water when thirsty, is a strong behavioral demand and associating the reward with its source, a certain environment or action, is paramount for survival. Here, we show that water reward increases subsequent visual activity in the superficial layers of the superior colliculus (SC), which receive direct input from the retina and belong to the earliest stages of visual processing. We trained mice of either sex to perform a visual decision task and recorded the activity of neurons in the SC using two-photon calcium imaging and high-density electrophysiological recordings. Responses to visual stimuli in around 20% of visually responsive neurons in the superficial SC were affected by reward delivered in the previous trial. Reward mostly increased visual responses independent from modulations due to pupil size changes. The modulation of visual responses by reward could not be explained by movements like licking. It was specific to responses to the following visual stimulus, independent of slow fluctuations in neural activity and independent of how often the stimulus was previously rewarded. Electrophysiological recordings confirmed these results and revealed that reward affected the early phase of the visual response around 80 ms after stimulus onset. Modulation of visual responses by reward, but not pupil size, significantly improved the performance of a population decoder to detect visual stimuli, indicating the relevance of reward modulation for the visual performance of the animal. To learn which actions lead to food, water, or safety, it is necessary to integrate the receiving of reward with sensory stimuli related to the reward. Cortical stages of sensory processing have been shown to represent stimulus-reward associations. Here, we show, however, that reward influences neurons at a much earlier stage of sensory processing, the superior colliculus (SC), receiving direct input from the retina. Visual responses were increased shortly after the animal received the water reward, which led to an improved stimulus signal in the population of these visual neurons. Reward modulation of early visual responses may thus improve perception of visual environments predictive of reward.
感觉输入的处理不断适应行为需求和内部状态。例如，获取奖励的动力（例如口渴时寻找水）是一种强烈的行为需求，将奖励与其来源（特定环境或动作）相关联对于生存至关重要。在这里，我们表明，水奖励会增加随后在高级视丘（SC）浅层的视觉活动，这些区域直接接收来自视网膜的输入，并且属于视觉处理的最早阶段。我们训练了雄性和雌性小鼠来执行视觉决策任务，并使用双光子钙成像和高密度电生理记录来记录 SC 中的神经元活动。在 SC 的浅层中，约 20%的对视觉有反应的神经元的视觉刺激反应受到前一次试验中给予的奖励的影响。奖励主要增加了与瞳孔大小变化引起的调制无关的视觉反应。奖励对视觉反应的调制不能用舔舐等运动来解释。它是对以下视觉刺激的反应特异性的，与神经活动的缓慢波动无关，也与刺激之前被奖励的频率无关。电生理记录证实了这些结果，并表明奖励会影响刺激后约 80 毫秒视觉反应的早期阶段。奖励对视觉反应的调制（而不是瞳孔大小）显著改善了用于检测视觉刺激的群体解码器的性能，表明奖励调制对动物的视觉性能具有重要意义。为了学习哪些动作会导致食物、水或安全，有必要将奖励的接收与与奖励相关的感官刺激结合起来。已经表明，皮质感觉处理阶段代表了刺激-奖励关联。然而，在这里，我们表明，奖励会影响到接收来自视网膜的直接输入的感觉处理的早期阶段，即高级视丘（SC）中的神经元。动物接受水奖励后不久，视觉反应就会增加，从而提高了这些视觉神经元群体中的刺激信号。因此，奖励对早期视觉反应的调制可能会改善对预测奖励的视觉环境的感知。
