Extracting 3D from Motion: Differences in Human and Monkey Intraparietal Cortex

Abstract

We compared three-dimensional structure-from-motion (3D-SFM) processing in awake monkeys and humans using functional magnetic resonance imaging. Occipital and midlevel extrastriate visual areas showed similar activation by 3D-SFM stimuli in both species. In contrast, intraparietal areas showed significant 3D-SFM activation in humans but not in monkeys. This suggests that human intraparietal cortex contains visuospatial processing areas that are not present in monkeys.To reconstruct the third dimension from a two-dimensional (2D) retinal image, our brain uses binocular as well as monocular cues such as shading, texture, and occlusion. Both humans and monkeys are also able to extract the 3D structure of an object from motion parallax cues that activate occipitoparietal areas in both species (1-3). Because neurons in the middle temporal area (MT/V5) are sensitive for speed gradients that reflect planes tilted in depth (4, see also 5), this area might play a crucial role in the extraction of depth from motion. Supporting evidence has been gleaned from a functional magnetic resonance imaging (fMRI) study showing 3D-SFM sensitivity in the human MT/V5 complex (hMT/V5ϩ) (6 ). These human fMRI results raise a first question: To what extent can they be generalized to the primate visual system? Furthermore, anatomical evidence suggests that there might be functional differences between human and monkey intraparietal cortex: The intraparietal sulcus separates area 5 from area 7 in the monkey, whereas in humans these two areas belong to the superior parietal lobe. In addition, in humans, the intraparietal lobe separates area 7 from areas 39 and 40, which have no clear counterpart in monkeys (7 ). Therefore, our second goal was to determine whether monkey intraparietal cortex is as important for motion-dependent depth processing as implied by human imaging (6 ).To address these issues, we turned to recently developed fMRI techniques (8) in awake (9-12) rather than anesthetized (13-14 ) monkeys. By performing human fMRI with virtually identical experimental procedures as in the awake monkey fMRI experiments, reliable interspecies comparisons could be made.The stimuli were displays of nine randomly connected lines, rotating in depth, that created a clear 3D percept (movie S1). Control stimuli consisted of the same displays that were either static or moving in one plane. We controlled for potential attentional differences between the 3D and 2D conditions by using a 1-back task in humans, as well as a demanding high-acuity fixation task (8, 9) in both species.In line with earlier reports (4-6, 13), area MT/V5 was activated more by 3D than by 2D moving random-line displays. In addition, the area in the fundus of the superior temporal sulcus (FST) also exhibited significant 3D-SFM sensitivity (Fig. 1A). Figure 2A shows the (3D -2D) pattern of activation for a single human subject, and the average activation for a group of eight subjects is shown in Fig. 2B. These results are similar to those obtained in an earlier study in which so...

Space representation for eye movements is more contralateral in monkeys than in humans

“…The correspondence between fMRI activation patterns in monkeys and humans in previous studies (e.g., [53][54][55][56][57][58] and, partly, in our work is encouraging, although it does not necessarily imply that the underlying behavioral strategies and neuronal activity in the two species are the same. Nevertheless, monkey fMRI provides a crucial control for the common interpretation of human imaging and monkey electrophysiology data.…”

The primary visual cortex fills in color

“…As previously mentioned, the mean performance of the attention task was 75 Ϯ 2% SE, indicating that the task was challenging (29,30).…”

“…To control attentional effects (29,30), we presented a small bar (0.3°) on the top of the fixation point and asked the subjects to perform an orientation indication task. In each trial, subjects were instructed to attend to a series of tiny vertical or horizontal bars presented intermittently near the fixation point throughout the test and control conditions.…”

“…To eliminate or decrease the attentional component of feedback signals, subjects performed an attentionally challenging task unrelated to the surface perception (29,30).…”

Neuroimaging Weighs In: Humans Meet Macaques in “Primate” Visual Cortex

“…1). These lower-tier areas are evolutionarily conserved in most mammals (Rosa and Krubitzer, 1999;Vanduffel et al, 2002).…”