Curvature-processing network in macaque visual cortex

Our visual environment abounds with curved features. Thus, the goal of understanding visual processing should include the processing of curved features. Using functional magnetic resonance imaging in behaving monkeys, we demonstrated a network of cortical areas selective for the processing of curved features. This network includes three distinct hierarchically organized regions within the ventral visual pathway: a posterior curvature-biased patch (PCP) located in the near-foveal representation of dorsal V4, a middle curvature-biased patch (MCP) located on the ventral lip of the posterior superior temporal sulcus (STS) in area TEO, and an anterior curvature-biased patch (ACP) located just below the STS in anterior area TE. Our results further indicate that the processing of curvature becomes increasingly complex from PCP to ACP. The proximity of the curvature-processing network to the well-known face-processing network suggests a possible functional link between them.Decades of research have focused on understanding visual feature processing, particularly along the ventral visual pathway. Such studies have shown that neurons in lower-order visual areas (e.g., V1) respond strongly to simple oriented contours (1), whereas neurons in higher-order visual areas (e.g., inferior temporal cortex) respond selectively to more complex image features and/or visual categories (2–4), in ways that are not yet fully understood. To link these extremes in visual information processing, many studies have aimed to clarify the optimal “trigger” features at intermediate levels of the visual cortical hierarchy.Among these features, stimulus curvature has not been well studied. This is surprising because, strictly, all lines are curved to some extent, except for the single exception of a perfectly straight line. This ubiquity of curved shapes also extends to 3D surfaces (5). In nature, where much of our visual system presumably evolved, perfectly flat surfaces are rare. Even the flattest of natural features (e.g., oceans, sandy beaches) are often curved to some extent, due to wind, water motion, and even the curvature of the earth. Thus, it is important to understand curvature processing to fully unravel the steps in cortical visual processing.Among the few studies to test single neuron responses to curvature per se, Gallant et al. (6, 7) reported that a significant percentage of neurons in macaque cortical area V4 is selective for curved stimuli. Intriguingly, these authors also noted that neurons preferring curved patterns were often anatomically clustered together. Subsequently, Pasupathy and Connor (8–10) demonstrated that neurons in the parafoveal representation of dorsal V4 respond robustly to the curvature component of complex shapes. To our knowledge, there have been no systematic studies of curvature at levels below V4 in macaques.Intriguingly, some evidence suggests that the processing of curvature may interact selectively with the processing of faces. For instance, perceptual deficits in face recognition (prosopagnosia) are sometimes associated with deficits in curvature discrimination (11). In addition, some neurons in face-selective regions of the temporal lobe also respond to rounded nonface objects (12, 13). A human functional magnetic resonance imaging (fMRI) study (14) reported that a concentrically curved grating produced a larger response in the fusiform face-selective area (FFA) (15, 16), compared with an otherwise identical linear grating.Here, we tested for a cortical specialization of curvature processing, using fMRI in fixating macaque monkeys. Given the previous single-unit studies (6–10), we expected that curved stimulus features would activate V4, either in specific patches or distributed throughout the area. The present fMRI approach also allowed us to test whether curvature processing is confined to V4, or whether it extends into additional brain regions. If specialized areas for curvature processing were identified, we could then ask whether they might be topographically linked with face-selective regions. Such an arrangement would shorten the mean axonal length between curvature- and face-processing regions, if these regions were functionally related.