How a sensory stimulus is processed and perceived depends on the surrounding sensory scene. In the visual cortex, contextual signals can be conveyed by an extensive network of intra- and inter-areal excitatory connections that link neurons representing stimulus features separated in visual space1–4. However, the connectional logic of visual contextual inputs remains unknown; it is not clear what information individual neurons receive from different parts of the visual field, nor how this input relates to the visual features a neuron encodes, defined by its spatial receptive field. We determined the organisation of excitatory synaptic inputs responding to different locations in the visual scene by mapping spatial receptive fields in dendritic spines of mouse visual cortex neurons using two-photon calcium imaging. We found that neurons received functionally diverse inputs from extended regions of visual space. Inputs representing similar visual features from the same location in visual space were more likely to cluster on neighbouring spines. Inputs from visual field regions beyond the postsynaptic neuron’s receptive field often synapsed on higher-order dendritic branches. These putative long-range inputs were more frequent and more likely to share the preference for oriented edges with the postsynaptic neuron when the input’s receptive field was spatially displaced along the axis of the postsynaptic neuron’s receptive field orientation. Therefore, the connectivity between neurons with displaced receptive fields obeys a specific rule, whereby they connect preferentially when their receptive fields are co-oriented and co-axially aligned. This organization of synaptic connectivity is ideally suited for amplification of elongated edges, which are enriched in the visual environment, and thus provides a potential substrate for contour integration and object grouping.

Visual intracortical and transthalamic pathways carry distinct information to cortical areasHighlights d Transthalamic pathway through pulvinar indirectly connects lower to higher cortical areas d This pathway combines input from V1 with that of many cortical and subcortical areas d Pulvinar conveys distinct visual and motor information to different higher visual areas d Direct intracortical and transthalamic pathways convey different information

Sensory processing involves information flow between neocortical areas, assumed to rely on direct intracortical projections. However, cortical areas may also communicate indirectly via higher-order nuclei in the thalamus, such as the pulvinar or lateral posterior nucleus (LP) in the visual system. The fine-scale organization and function of these cortico-thalamo-cortical pathways remains unclear. We find that responses of mouse LP neurons projecting to higher visual areas likely derive from feedforward input from primary visual cortex (V1) combined with information from many cortical and subcortical areas, including superior colliculus. Signals from LP projections to different higher visual areas are tuned to specific features of visual stimuli and their locomotor context, distinct from the signals carried by direct intracortical projections from V1. Thus, visual transthalamic pathways are functionally specific to their cortical target, different from feedforward cortical pathways and combine information from multiple brain regions, linking sensory signals with behavioral context.