Ilse Van Dromme

Responses to two-dimensional shapes in the macaque anterior intraparietal area

Neurons in the macaque dorsal visual stream respond to the visual presentation of objects in the context of a grasping task and to three‐dimensional (3D) surfaces defined by binocular disparity, but little is known about the neural representation of two‐dimensional (2D) shape in the dorsal stream. We recorded the activity of single neurons in the macaque anterior intraparietal area (AIP), which is known to be crucial for grasping, during the presentation of images of objects and silhouette, outline and line‐drawing versions of these images (contour stimuli). The vast majority of AIP neurons responding selectively to 2D images were also selective for at least one of the contour stimuli with the same boundary shape, suggesting that the boundary is sufficient for the image selectivity of most AIP neurons. Furthermore, a subset of these neurons with foveal receptive fields generally preserved the shape preference across positions, whereas for more than half of the AIP population the center of the receptive field was at a parafoveal location with less tolerance to changes in stimulus position. AIP neurons frequently exhibited shape selectivity across different stimulus sizes. These results demonstrate that AIP neurons encode not only 3D but also 2D shape features.

Posterior Parietal Cortex Drives Inferotemporal Activations During Three-Dimensional Object Vision

The primate visual system consists of a ventral stream, specialized for object recognition, and a dorsal visual stream, which is crucial for spatial vision and actions. However, little is known about the interactions and information flow between these two streams. We investigated these interactions within the network processing three-dimensional (3D) object information, comprising both the dorsal and ventral stream. Reversible inactivation of the macaque caudal intraparietal area (CIP) during functional magnetic resonance imaging (fMRI) reduced fMRI activations in posterior parietal cortex in the dorsal stream and, surprisingly, also in the inferotemporal cortex (ITC) in the ventral visual stream. Moreover, CIP inactivation caused a perceptual deficit in a depth-structure categorization task. CIP-microstimulation during fMRI further suggests that CIP projects via posterior parietal areas to the ITC in the ventral stream. To our knowledge, these results provide the first causal evidence for the flow of visual 3D information from the dorsal stream to the ventral stream, and identify CIP as a key area for depth-structure processing. Thus, combining reversible inactivation and electrical microstimulation during fMRI provides a detailed view of the functional interactions between the two visual processing streams.

Effective connectivity of depth-structure-selective patches in the lateral bank of the macaque intraparietal sulcus.

Extrastriate cortical areas are frequently composed of subpopulations of neurons encoding specific features or stimuli, such as color, disparity, or faces, and patches of neurons encoding similar stimulus properties are typically embedded in interconnected networks, such as the attention or face-processing network. The goal of the current study was to examine the effective connectivity of subsectors of neurons in the same cortical area with highly similar neuronal response properties. We first recorded single- and multi-unit activity to identify two neuronal patches in the anterior part of the macaque intraparietal sulcus (IPS) showing the same depth structure selectivity and then employed electrical microstimulation during functional magnetic resonance imaging in these patches to determine the effective connectivity of these patches. The two IPS subsectors we identified—with the same neuronal response properties and in some cases separated by only 3 mm—were effectively connected to remarkably distinct cortical networks in both dorsal and ventral stream in three macaques. Conversely, the differences in effective connectivity could account for the known visual-to-motor gradient within the anterior IPS. These results clarify the role of the anterior IPS as a pivotal brain region where dorsal and ventral visual stream interact during object analysis. Thus, in addition to the anatomical connectivity of cortical areas and the properties of individual neurons in these areas, the effective connectivity provides novel key insights into the widespread functional networks that support behavior.

The Role of Binocular Disparity in Stereoscopic Images of Objects in the Macaque Anterior Intraparietal Area

Neurons in the macaque Anterior Intraparietal area (AIP) encode depth structure in random-dot stimuli defined by gradients of binocular disparity, but the importance of binocular disparity in real-world objects for AIP neurons is unknown. We investigated the effect of binocular disparity on the responses of AIP neurons to images of real-world objects during passive fixation. We presented stereoscopic images of natural and man-made objects in which the disparity information was congruent or incongruent with disparity gradients present in the real-world objects, and images of the same objects where such gradients were absent. Although more than half of the AIP neurons were significantly affected by binocular disparity, the great majority of AIP neurons remained image selective even in the absence of binocular disparity. AIP neurons tended to prefer stimuli in which the depth information derived from binocular disparity was congruent with the depth information signaled by monocular depth cues, indicating that these monocular depth cues have an influence upon AIP neurons. Finally, in contrast to neurons in the inferior temporal cortex, AIP neurons do not represent images of objects in terms of categories such as animate-inanimate, but utilize representations based upon simple shape features including aspect ratio.

The relation between functional magnetic resonance imaging activations and single-cell selectivity in the macaque intraparietal sulcus

Previous functional magnetic resonance (fMRI) studies in humans and monkeys have demonstrated that the anterior intraparietal sulcus (IPS) is sensitive to the depth structure defined by binocular disparity. However, in the macaque monkey, a single large activation was measured in the anterior lateral bank of the IPS, whereas in human subjects two separate regions were sensitive to depth structure from disparity. We performed fMRI and single-cell experiments in the same animals, in a large number of recording sites in the lateral bank of the IPS. The fMRI interaction effect between the factors curvature (curved or flat) and disparity (stereo or control) correctly predicted the location of higher-order disparity selective neurons that encoded the depth structure of objects. However the large region in the IPS activated by depth structure consisted of two patches of higher-order disparity-selective neurons, one in the anterior IPS and one located more posteriorly, surrounded by regions lacking such selectivity. Thus the IPS region activated by curved surfaces consists of at least two patches of higher-order disparity selective neurons, which may reconcile previous fMRI studies in monkeys and humans.

Caudal Intraparietal Sulcus and three-dimensional vision: A combined functional magnetic resonance imaging and single-cell study

&NA; The cortical network processing three‐dimensional (3D) object structure defined by binocular disparity spans both the ventral and dorsal visual streams. However, very little is known about the neural representation of 3D structure at intermediate levels of the visual hierarchy. Here, we investigated the neural selectivity for 3D surfaces in the macaque Posterior Intraparietal area (PIP) in the medial bank of the caudal intraparietal sulcus (IPS). We first identified a region sensitive to depth‐structure information in the medial bank of the caudal IPS using functional Magnetic Resonance Imaging (fMRI), and then recorded single‐cell activity within this fMRI activation in the same animals. Most PIP neurons were selective for the 3D orientation of planar surfaces (first‐order disparity) at very short latencies, whereas a very small fraction of PIP neurons were selective for curved surfaces (second‐order disparity). A linear support vector machine classifier could reliably identify the direction of the disparity gradient in planar and curved surfaces based on the responses of a population of disparity‐selective PIP neurons. These results provide the first detailed account of the neuronal properties in area PIP, which occupies an intermediate position in the hierarchy of visual areas involved in processing depth structure from disparity. HighlightsThe selectivity for 3D stimuli in PIP consists of zero‐and first‐order neurons and a small percentage of second‐order neurons.The representation of depth structure at the population level, however, is largely higher order.PIP cells tolerate size variations and have parafoveal multi‐focal receptive fields.PIP may be one of the earliest higher‐order disparity‐processing areas in the dorsal stream.

Single-cell responses to three-dimensional structure in a functionally-defined patch in macaque area TEO

Both dorsal and ventral visual pathways harbor several areas sensitive to gradients of binocular disparity (i.e., higher-order disparity). Although a wealth of information exists about disparity processing in early visual (V1, V2, and V3) and end-stage areas, TE in the ventral stream, and the anterior intraparietal area (AIP) in the dorsal stream, little is known about midlevel area TEO in the ventral pathway. We recorded single-unit responses to disparity-defined curved stimuli in a functional magnetic resonance imaging (fMRI) activation elicited by curved surfaces compared with flat surfaces in the macaque area TEO. This fMRI activation contained a small proportion of disparity-selective neurons, with very few of them second-order disparity selective. Overall, this population of TEO neurons did not preserve its three-dimensional structure selectivity across positions in depth, indicating a lack of higher-order disparity selectivity, but showed stronger responses to flat surfaces than to curved surfaces, as predicted by the fMRI experiment. The receptive fields of the responsive TEO cells were relatively small and generally foveal. A linear support vector machine classifier showed that this population of disparity-selective TEO neurons contains reliable information about the sign of curvature and the position in depth of the stimulus. NEW & NOTEWORTHY We recorded in a part of the macaque area TEO that is activated more by curved surfaces than by flat surfaces at different disparities using the same stimuli. In contrast to previous studies, this functional magnetic resonance imaging-defined patch did not contain a large number of higher-order disparity-selective neurons. However, a linear support vector machine could reliably classify both the sign of the disparity gradient and the position in depth of the stimuli.