Orientation-tuned surround suppression exhibits a unique laminar signature in human primary visual cortex

Spatial context modifies visual perception by enhancing novel and salient features over spatially redundant features in the underlying neural code of primary visual cortex (V1). Although multiple intracortical pathways contribute to contextual modulation, their specific contributions to different types of contextual modulation are not fully understood. Leveraging the distinct laminar connectivity patterns of feedforward, feedback, and lateral pathways, we used ultra-high-resolution fMRI (7T T2*-weighted, 0.6 mm isotropic resolution) to infer their relative contributions to contextual modulation in V1 by analyzing blood-oxygenation-level-dependent (BOLD) signal across cortical depth. Participants viewed sine-wave grating disks embedded in large surround gratings. Segmentation cues were introduced or removed by manipulating the relative phase and orientation of the surround gratings, yielding three contextual conditions and a surround-only condition to measure the effects of context in the absence of feedforward input. Our analysis isolated the effects of orientation-tuned surround suppression (OTSS) from orientation-independent border-induced modulation (BIM). The results show that BOLD laminar profiles differ by modulation type: BIM affected both deep and superficial voxels, while OTSS was absent in deep voxels. We also find that voxels at all depths are driven by spatial context in the absence of feedforward input, which accords with the discovery of contextually-driven neural responses in mammalian V1. These laminar differences likely reflect distinct contributions of feedback from higher-order visual areas and long-range lateral connections within V1. Our findings help to explicate the contributions of recurrent processing in visual contextual modulation and demonstrate the participation of lateral pathways in laminar-dependent BOLD fMRI. Significance StatementContextual modulation integrates visual information across spatial scales, guided by intracortical lateral and feedback connections in primary visual cortex (V1). However, the independent contributions of these pathways to distinct contextual phenomena remain unclear. Using laminar functional magnetic resonance imaging (fMRI), we investigated how these pathways process different types of contextual features. Blood-oxygenation-level-dependent (BOLD) laminar profiles varied with the type of visual context, indicating distinct intracortical pathways are involved in processing specific contextual features. These findings enhance our understanding of the mechanisms underlying human vision and provide evidence that V1-intrinsic lateral connections exhibit unique laminar signatures in the BOLD signal.