Pivotal role of hMT+ in long‐range disambiguation of interhemispheric bistable surface motion

Abstract

It remains an open question whether long-range disambiguation of ambiguous surface motion can be achieved in early visual cortex or instead in higher level regions, which concerns object/surface segmentation/integration mechanisms. We used a bistable moving stimulus that can be perceived as a pattern comprehending both visual hemi-fields moving coherently downward or as two widely segregated nonoverlapping component objects (in each visual hemi-field) moving separately inward. This paradigm requires long-range integration across the vertical meridian leading to interhemispheric binding. Our fMRI study (n = 30) revealed a close relation between activity in hMT+ and perceptual switches involving interhemispheric segregation/integration of motion signals, crucially under nonlocal conditions where components do not overlap and belong to distinct hemispheres. Higher signal changes were found in hMT+ in response to spatially segregated component (incoherent) percepts than to pattern (coherent) percepts. This did not occur in early visual cortex, unlike apparent motion, which does not entail surface segmentation. We also identified a role for top-down mechanisms in state transitions. Deconvolution analysis of switch-related changes revealed prefrontal, insula, and cingulate areas, with the right superior parietal lobule (SPL) being particularly involved. We observed that directed influences could emerge either from left or right hMT+ during bistable motion integration/segregation. SPL also exhibited significant directed functional connectivity with hMT+, during perceptual state maintenance (Granger causality analysis). Our results suggest that long-range interhemispheric binding of ambiguous motion representations mainly reflect bottom-up processes from hMT+ during perceptual state maintenance. In contrast, state transitions maybe influenced by high-level regions such as the SPL. Hum Brain Mapp 38:4882-4897, 2017. © 2017 Wiley Periodicals, Inc.

Tracking perceptual decision mechanisms through changes in interhemispheric functional connectivity in human visual cortex

“…There is single-cell electrophysiological evidence that neuronal computation of global 2-D or pattern motion is performed by such pattern selective neurons in hMT+, while neurons in early visual cortex, such as V1 and V2, are only sensitive to 1-D motion features of an object (virtually 100% of component motion neurons in these regions) 18,19 . It is therefore not expected that V1 and V2 differentially respond to stimuli requiring perceptual integration, as we have verified in our previous studies 13,15 .…”

“…This allows us to specifically investigate the role of the hMT+ interhemispheric functional connectivity in the modulation of surface segregation vs. integration as a probe to investigate the role long-range interactions in decision. In a previous study we observed that long-range binding of this bistable stimulus mainly reflect bottom-up processes arising within hMT+ 13 . As a step further, we set to investigate with high-resolution (7T) functional magnetic resonance imaging (fMRI), the role of interhemispheric functional connectivity across hMT+ in both hemispheres as a modulator of perceptual integration vs. segregation of multiple physically constant moving surfaces separated across hemifields.…”

“…In any case, evidence from functional connectivity data that an early visual area such as hMT+ can be pivotal in perceptual binding across hemispheres has so far been absent. If this hypothesis holds true, it would also inform the independent debate concerning bottom-up vs. top-down mechanisms in perceptual decision 13 . Moreover, structural connectivity data from callosal segments connecting hMT+ show a correlation with perceived horizontal apparent motion 12 .…”

“…To take advantage of the high-dimensional nature of 7T fMRI data we acquired a slab of data focused on hMT+ (although covering also other visual areas). This a priori choice of our region of interest was based on our own previous findings using fMRI data 13 , suggesting a role for this complex and heterogeneous region (containing MT proper and MST) in perceptual disambiguation of moving surfaces. Previously, we have found that hMT+ has a bottom-up dominant role during long-range binding and is critical for the maintenance of the perceptual representations (other areas were only involved during the short switch events) 13,15 .…”

“…This a priori choice of our region of interest was based on our own previous findings using fMRI data 13 , suggesting a role for this complex and heterogeneous region (containing MT proper and MST) in perceptual disambiguation of moving surfaces. Previously, we have found that hMT+ has a bottom-up dominant role during long-range binding and is critical for the maintenance of the perceptual representations (other areas were only involved during the short switch events) 13,15 . Furthermore, previous studies using EEG and structural MRI data had proposed that perceptual decision can be indexed in interhemispheric hMT+ communication 11,12 , reinforcing our a priori hypothesis.…”