Partial information transfer from peripheral visual streams to foveal visual streams is mediated through local primary visual circuits

Abstract

A classic view holds that visual object recognition is driven through the what pathway in which perceptual features of increasing abstractness are computed in a sequence of different visual cortical regions. The cortical origin of this pathway, the primary visual cortex (V1), has a retinotopic organization such that neurons have receptive fields tuned to specific regions of the visual field. That is, a neuron that responds to a stimulus in the center of the visual field will not respond to a stimulus in the periphery of the visual field, and vice versa. However, despite this fundamental design feature, the overall processing of stimuli in the periphery - while clearly dependent on processing by neurons in the peripheral regions of V1 - can be clearly altered by the processing of neurons in the fovea region of V1. For instance, it has been shown that task-relevant, non-retinotopic feedback information about peripherally presented stimuli can be decoded in the unstimulated foveal cortex, and that the disruption of this feedback - through Transcranial Magnetic Stimulation or behavioral masking paradigms - has detrimental effects on same/different discrimination behavior. Here, we used fMRI multivariate decoding techniques and functional connectivity analyses to assess the nature of the information that is encoded in the periphery-to-fovea feedback projection and to gain insight into how it may be anatomically implemented. Participants performed a same/different discrimination task on images of real-world stimuli (motorbikes, cars, female and male faces) displayed peripherally. We were able to decode only a subset of these categories from the activity measured in peripheral V1, and a further reduced subset from the activity measured in foveal V1, indicating that the feedback from periphery to fovea may be subject to information loss. Functional connectivity analysis revealed that foveal V1 was functionally connected only to the peripheral V1 and not to later-stage visual areas, indicating that the feedback from peripheral to foveal V1 is likely implemented by neural circuits local to V1.