Werner Reichardt Centre for Integrative Neuroscience, University of Tübingen, Tübingen 72076, Germany.
Graduate Training Centre of Neuroscience, International Max Planck Research School, Tübingen 72076, Germany.
J Neurosci. 2021 Apr 14;41(15):3531-3544. doi: 10.1523/JNEUROSCI.1828-20.2021. Epub 2021 Mar 9.
Choosing an action in response to visual cues relies on cognitive processes, such as perception, evaluation, and prediction, which can modulate visual representations even at early processing stages. In the mouse, it is challenging to isolate cognitive modulations of sensory signals because concurrent overt behavior patterns, such as locomotion, can also have brainwide influences. To address this challenge, we designed a task, in which head-fixed mice had to evaluate one of two visual cues. While their global shape signaled the opportunity to earn reward, the cues provided equivalent local stimulation to receptive fields of neurons in primary visual (V1) and anterior cingulate cortex (ACC). We found that mice evaluated these cues within few hundred milliseconds. During this period, ∼30% of V1 neurons became cue-selective, with preferences for either cue being balanced across the recorded population. This selectivity emerged in response to the behavioral demands because the same neurons could not discriminate the cues in sensory control measurements. In ACC, cue evaluation affected a similar fraction of neurons; emerging selectivity, however, was stronger than in V1, and preferences in the recorded population were biased toward the cue promising reward. Such a biased selectivity regime might allow the mouse to infer the promise of reward simply by the overall level of activity. Together, these experiments isolate the impact of task demands on neural responses in mouse cerebral cortex, and document distinct neural signatures of cue evaluation in V1 and ACC. Performing a cognitive task, such as evaluating visual cues, not only recruits frontal and parietal brain regions, but also modulates sensory processing stages. We trained mice to evaluate two visual cues, and show that, during this task, ∼30% of neurons recorded in V1 became selective for either cue, although they provided equivalent visual stimulation. We also show that, during cue evaluation, mice frequently move their eyes, even under head fixation, and that ignoring systematic differences in eye position can substantially obscure the modulations seen in V1 neurons. Finally, we document that modulations are stronger in ACC, and biased toward the reward-predicting cue, suggesting a transition in the neural representation of task-relevant information across processing stages in mouse cerebral cortex.
选择对视觉线索做出反应的行动依赖于认知过程，如感知、评估和预测，这些过程甚至可以在早期处理阶段调节视觉表示。在小鼠中，由于并发的明显行为模式（如运动）也会对大脑产生广泛影响，因此很难分离出对感觉信号的认知调节。为了解决这个挑战，我们设计了一个任务，在这个任务中，头部固定的老鼠必须评估两个视觉线索中的一个。虽然它们的整体形状表示有机会获得奖励，但这些线索为初级视觉 (V1) 和前扣带皮层 (ACC) 的神经元提供了等效的局部刺激。我们发现，老鼠在几百毫秒内评估了这些线索。在此期间，约 30%的 V1 神经元变得对线索有选择性，在记录的群体中，对两个线索的偏好是平衡的。这种选择性是针对行为需求而出现的，因为相同的神经元不能在感觉控制测量中区分线索。在 ACC 中，线索评估影响了类似比例的神经元；然而，出现的选择性比 V1 更强，记录群体中的偏好偏向于承诺奖励的线索。这种偏向性选择性机制可能使老鼠仅通过整体活动水平就能推断出奖励的承诺。总的来说，这些实验在小鼠大脑皮层中分离了任务需求对神经反应的影响，并记录了 V1 和 ACC 中线索评估的不同神经特征。执行认知任务，如评估视觉线索，不仅会招募额叶和顶叶脑区，还会调节感觉处理阶段。我们训练老鼠评估两个视觉线索，并表明，在这个任务中，尽管记录的 V1 中约 30%的神经元对两个线索都有选择性，但它们提供了等效的视觉刺激。我们还表明，在评估线索时，即使在头部固定的情况下，老鼠也经常转动眼睛，并且忽略眼位的系统差异会大大掩盖 V1 神经元中的调制。最后，我们记录到，在 ACC 中，调制更强，并且偏向于预测奖励的线索，这表明在小鼠大脑皮层中，与任务相关信息的神经表示在处理阶段发生了转变。
