Attention modulates neuronal correlates of interhemispheric integration and global motion perception

Abstract

In early retinotopic areas of the human visual system, information from the left and right visual hemifields (VHFs) is processed contralaterally in two hemispheres. Despite this segregation, we have the perceptual experience of a unified, coherent, and uninterrupted single visual field. How exactly the visual system integrates information from the two VHFs and achieves this perceptual experience still remains largely unknown. In this study using fMRI, we explored candidate areas that are involved in interhemispheric integration and the perceptual experience of a unified, global motion across VHFs. Stimuli were two-dimensional, computer-generated objects with parts in both VHFs. The retinal image in the left VHF always remained stationary, but in the experimental condition, it appeared to have local motion because of the perceived global motion of the object. This perceptual effect could be weakened by directing the attention away from the global motion through a demanding fixation task. Results show that lateral occipital areas, including the medial temporal complex, play an important role in the process of perceptual experience of a unified global motion across VHFs. In early areas, including the lateral geniculate nucleus and V1, we observed correlates of this perceptual experience only when attention is not directed away from the object. These findings reveal effects of attention on interhemispheric integration in motion perception and imply that both the bilateral activity of higher-tier visual areas and feedback mechanisms leading to bilateral activity of early areas play roles in the perceptual experience of a unified visual field.

Keywords: fMRI; global motion perception; interhemispheric integration; perceptual experience of unified visual field; visual brain.

Figure 1

Stimuli used in fMRI experiments. When the Pac-man figure oscillates about the axis going through its center, the whole figure seems to oscillate even though the motion signals are only around its “mouth.” Importantly, when the oscillations are such that the local signals are confined to the right visual field, the part of the figure in the left visual field is still perceived as oscillating. In the control stimulus, in which a wedge on the right visual field oscillates, the left part of the figure appears static. Note that the local motion-dependent energy signals are approximately the same across the two conditions.

Figure 2

Experimental protocol and stimulus details. Responses to dynamic Pac-man and control stimuli were measured using a block design protocol. In each experimental run, a 12-s presentation of static stimulus was followed by 12 s of a dynamic block in which the figure oscillated about its center. This sequence was repeated 10 times in a run. In order to control for the effects of attention, observers were required to perform a demanding fixation task. In another condition, they passively viewed the stimulus while maintaining fixation at the central mark.

Figure 3

ROIs were identified using wedges texture-mapped with counter-phase contrast reversing checkerboard patterns in early visual areas (the Pac-man figure in the background is shown here for visualization purposes; it was not present in the actual experiment). For MT+, moving random dots were used as a localizer. Boundaries between early visual areas were drawn using the results of a separate retinotopic mapping session for each participant. The image on the right shows ROIs and visual area boundaries on an inflated brain of one participant.

Figure 4

Possible outcomes. If the activity in a visual area is determined solely by localized motion signals on the retina, then we would expect approximately equal activity in that area under both stimulus conditions. This possibility is shown as the null hypothesis in the first row of functional plots. The common activity in the right hemisphere may be either vanishingly small (small RFs, restricted to contralateral VHF) or nonzero (large RFs, expanding into ipsilateral VHF). Alternatively, if the activity of an area depends on the perceived motion of an object unified across visual fields and not only on the localized physical motion signals, then we would expect a larger signal in the right hemisphere for the Pac-man condition than for the control condition. This possibility is presented in the last row. In both the null and alternative hypotheses, we would expect the activity in an area in the left hemisphere to be roughly equal in the Pac-man and control conditions because the local motion energy signals are approximately the same in the right VHF.

Figure 5

Event-related averages across all observers and all runs. Time point zero indicates the onset of the dynamic block. Red lines show the responses to the Pac-man stimulus; black lines show responses to the control stimulus. Error bars represent the 95% confidence interval. Note that in both conditions we often measured negative fMRI signal in right V1, V2, and V3. This kind of ipsilateral negative activity is consistent with earlier reports in literature.

Figure 5

Continued.

Figure 6

Difference between Pac-man and control conditions in the right hemisphere. The bars show the difference between the averaged signals from 8 to 12 s after the onset of the dynamic blocks for the Pac-man and control stimuli. Error bars are 95% confidence interval. A “*” indicates significance at α = 0.05 level. Dorsolateral occipital areas are differentially more active during the presentation of oscillating Pac-man stimulus than that of control stimulus in both the passive-view and fixation-task conditions whereas early visual areas, including LGN, are differentially more active only in the passive-view condition.