Experience-dependent predictions of feedforward and contextual information in mouse visual cortex

ABSTRACT Neurons in primary visual cortex are driven by feedforward visual inputs and top-down contextual inputs. The nature of this contextual information is difficult to study, as responses to feedforward and top-down inputs overlap in time and are difficult to disentangle experimentally. To address this issue, we measured responses to natural images and partially occluded versions of these images in the visual cortex of mice. Assessing neuronal responses before and after familiarizing mice with the non-occluded images allowed us to study experience-dependent and stimulus-specific contextual responses in pyramidal cells (PyCs) in cortical layers 2/3 and 5 in the absence of feedforward input. Surprisingly, in the same retinotopic region of cortex, we found that separate populations of PyCs in layer 2/3 responded to occluded and non-occluded images. Responses of PyCs selective for occluded images were strengthened upon familiarization and decoding analysis revealed they contained image-specific information, suggesting that they signaled the absence of predicted visual stimuli. Responses of PyCs selective for non-occluded scenes were weaker for familiarized images but stronger for unfamiliar images, suggesting that these neurons signaled the presence of unpredicted visual stimuli. Layer 5 also contained PyCs preferring either feedforward or contextual inputs, but their responses were more complex and strengthening of responses to occluded images required task engagement. The results show that visual experience decreases the activity of neurons responding to known feedforward inputs but increases the activity of neurons responding to contextual inputs tied to expected stimuli.