Selective stimulation of neurons in visual cortex enables segregation of slow and fast connections

Abstract

Organization of the central visual pathway is generally studied from a perspective of feedforward processes. However, there are horizontal connections and also strong feedback from extra striate to visual cortex. Here, we use visual stimuli designed to maximize relative differential involvements of these three main types of connections. The approach relies on differences between stimulation within the classical receptive field (CRF) and that of the surround region. Although previous studies have used similar approaches, they were limited primarily to spatial segregation of neural connections. Our experimental design provides clear segregation of fast and slow components of surround modulation. We assume these are mediated by feedback and horizontal connections, respectively, but other factors may be involved. Our results imply that both horizontal and feedback connections contribute to integration of visual information outside the CRF and provide suppressive or facilitative modulation. For a given cell, modulation may change in strength and sign from suppression to facilitation or the reverse depending on surround parameters. Sub-threshold input from the CRF surround increases local field potential (LFP) power in distinct frequency ranges which differ for suppression and facilitation. Horizontal connections have delayed CRF-surround modulation and are sensitive to position changes in the surround. Therefore, surround information beyond the CRF is initially processed by fast connections which we consider to be feedback, whereas spatially tuned mechanisms are relatively slow and presumably mediated by horizontal connections. Overall, results suggest that convergent fast (feedforward) inputs determine size and structure of the CRFs of recipient cells in visual cortex. And fast connections from extra striate regions (feedback) plus slow-tuned connections (horizontal) within visual cortex contribute to spatial influences of CRF surround activation.