A Distinct Representation of Three-Dimensional Shape in Macaque Anterior Intraparietal Area: Fast, Metric, and Coarse

Abstract

Differences in the horizontal positions of retinal images-binocular disparity-provide important cues for three-dimensional object recognition and manipulation. We investigated the neural coding of three-dimensional shape defined by disparity in anterior intraparietal (AIP) area. Robust selectivity for disparity-defined slanted and curved surfaces was observed in a high proportion of AIP neurons, emerging at relatively short latencies. The large majority of AIP neurons preserved their three-dimensional shape preference over different positions in depth, a hallmark of higher-order disparity selectivity. Yet both stimulus type (concave-convex) and position in depth could be reliably decoded from the AIP responses. The neural coding of three-dimensional shape was based on first-order (slanted surfaces) and second-order (curved surfaces) disparity selectivity. Many AIP neurons tolerated the presence of disparity discontinuities in the stimulus, but the population of AIP neurons provided reliable information on the degree of curvedness of the stimulus. Finally, AIP neurons preserved their three-dimensional shape preference over different positions in the frontoparallel plane. Thus, AIP neurons extract or have access to three-dimensional object information defined by binocular disparity, consistent with previous functional magnetic resonance imaging data. Unlike the known representation of three-dimensional shape in inferior temporal cortex, the neural representation in AIP appears to emphasize object parameters required for the planning of grasping movements.

Selectivity for Three-Dimensional Shape and Grasping-Related Activity in the Macaque Ventral Premotor Cortex

“…2A) filled with a 50% density random dot pattern (stimulus size, 5.5°). Consistent with previous studies (Janssen et al, 2000b;Srivastava et al, 2009), we will refer to the combination of a 2D contour and a depth profile as a "3D shape." On the basis of the responses in this test, the optimal 2D contour and two depth profiles (one of which the neuron responded strongly to, plus a less effective depth profile) were selected and further tested in a disparity test.…”

“…The surgical and recording procedures were similar to previous experiments (Janssen et al, 1999(Janssen et al, , 2000bSrivastava et al, 2009). Under isoflurane anesthesia, an MRI-compatible head fixation post and recording chamber were implanted using dental acrylic and ceramic screws.…”

“…Two male rhesus monkeys (M1 and M2) served as subjects for extracellular microelectrode recordings [M2 was also used in the study by Srivastava et al (2009) on AIP]. The surgical and recording procedures were similar to previous experiments (Janssen et al, 1999(Janssen et al, , 2000bSrivastava et al, 2009).…”

“…The stimulus set was identical to those used in previous experiments in AIP (Srivastava et al, 2009;Joly et al, 2009) and consisted of 32 3D shapes portraying curved surfaces, in which four disparity profiles were imposed over eight 2D contours ( Fig. 2A) filled with a 50% density random dot pattern (stimulus size, 5.5°).…”

“…Srivastava et al (2009) showed that a subset of neurons in area AIP encode the depth profile of curved surfaces defined by disparity (i.e., higher-order disparity selective). Since AIP and F5a are strongly interconnected as parts of the parietofrontal grasping circuit (Nelissen and Vanduffel, 2011), and in view of the fMRI results of Joly et al (2009), we wanted to determine whether individual F5a neurons were indeed higher-order disparity selective, similar to neurons in area AIP (Srivastava et al, 2009) and inferior temporal cortex (IT) (Janssen et al, 1999). Furthermore, we characterized 3D-shape-selective F5a neurons during grasping in the light and in the dark.…”