Psychophysical and neuroimaging responses to moving stimuli in a patient with the Riddoch phenomenon due to bilateral visual cortex lesions

Abstract

Patients with injury to early visual cortex or its inputs can display the Riddoch phenomenon: preserved awareness for moving but not stationary stimuli. We provide a detailed case report of a patient with the Riddoch phenomenon, MC. MC has extensive bilateral lesions to occipitotemporal cortex that include most early visual cortex and complete blindness in visual field perimetry testing with static targets. Nevertheless, she shows a remarkably robust preserved ability to perceive motion, enabling her to navigate through cluttered environments and perform actions like catching moving balls. Comparisons of MC's structural magnetic resonance imaging (MRI) data to a probabilistic atlas based on controls reveals that MC's lesions encompass the posterior, lateral, and ventral early visual cortex bilaterally (V1, V2, V3A/B, LO1/2, TO1/2, hV4 and VO1 in both hemispheres) as well as more extensive damage to right parietal (inferior parietal lobule) and left ventral occipitotemporal cortex (VO1, PHC1/2). She shows some sparing of anterior occipital cortex, which may account for her ability to see moving targets beyond ~15 degrees eccentricity during perimetry. Most strikingly, functional and structural MRI revealed robust and reliable spared functionality of the middle temporal motion complex (MT+) bilaterally. Moreover, consistent with her preserved ability to discriminate motion direction in psychophysical testing, MC also shows direction-selective adaptation in MT+. A variety of tests did not enable us to discern whether input to MT+ was driven by her spared anterior occipital cortex or subcortical inputs. Nevertheless, MC shows rich motion perception despite profoundly impaired static and form vision, combined with clear preservation of activation in MT+, thus supporting the role of MT+ in the Riddoch phenomenon.

Keywords: Blindsight; FMRI; Middle temporal area (MT+); Motion perception; Riddoch phenomenon; Vision.

Fig. 1.. Extent of lesion.

(A) Sagittal slices from MC’s T1-weighted anatomical scans. MC’s lesion included most of occipital cortex bilaterally as well as posterior temporal cortex bilaterally and right parietal cortex. (B) MC’s lesion (grey shading) projected onto an MNI surface with probabilistic estimates of 21 retinotopic areas defined in neurologically intact participants (solid white lines). MC’s lesion was classified into regions with that were completely lesioned and lacked any identifiable tissue (darker transparent grey with black outline) and regions with abnormal tissue or atrophy (lighter transparent grey with black outline). MC’s lesion encompassed early visual areas V1-V3 as well as extrastriate areas hV4, V3A, V3B, LO1–2, and VO1.

Fig. 2.. Motion responses in MT+ for looming/receding vs. static checkerboards.

(A) MC was scanned while viewing 16-s blocks of a static checkerboard, a looming/receding checkerboard and a blank screen. A contrast of moving > stationary revealed strong activation in dorsal and ventral subregions of MT+ in both hemispheres. Slice planes are specified in Talairach coordinates and indicated by dashed lines in orthogonal slices. (B) Time courses of activation extracted from subregions in A show the expected rise in activation with the onset of motion and decline with the offset, consistent with the hemodynamic response function. Activation was particularly robust in left dorsal MT+.

Fig. 3.. Visual responses in anterior calcarine cortex for visual checkerboards vs. a blank screen.

(A) A contrast of moving and stationary checkerboards vs. a blank screen revealed activation in anterior calcarine cortex, just posterior to the intersection of the calcarine sulcus with the parieto-occipital sulcus. This region showed no statistically significant difference between moving and static checkerboards. Slice planes are specified in Talairach coordinates and indicated by thin black dashed lines in orthogonal slices. The parieto-occipital is indicated by solid white line. The calcarine sulcus is indicated by dashed white line. (B) The time course of activation extracted from the region in A shows the expected rise in activation with the onset of checkerboard stimuli and decline with the offset, consistent with the hemodynamic response function.

Fig. 4.. MC’s perimetry and visual field responsiveness.

We combined probabilistic retinotopic maps (polar angle on the left and eccentricity on the right) from an atlas based on neurologically intact participants (A) with MC’s visually evoked activity for flickering checkerboard stimuli (shown in orange in (B)). The comparison suggested that MC may have spared vision in the upper left visual field beyond ~12°(C) consistent with her perimetry data (D, modified from data in Thaler et al., 2016), which indicated sparing of sensitivity for moving (but not static) targets within the upper left visual field beyond ~10°.

Fig. 5.. Motion direction selectivity.

(A) MC viewed blocks in which coarse RDKs moved in the same direction on every trial (adapted condition) or changed from trial to trial (non-adapted condition) in 16-s blocks. (B) Significantly greater activity to moving vs. static dots was observed within right dorsal and ventral MT+ (as well as right ventral MT+, not shown) (p < 0.01, uncorrected). (C) In right ventral MT+, activation was significantly higher for non-adapted vs. adapted motion blocks, a signature of direction selectivity. Vertical dashed line marks stimulus onset. Shaded region illustrates SEM across blocks. (D) Sensitivity to motion direction observed in dorsal subdivision of MT+ bilaterally as well as motion-sensitive regions of the intraparietal sulcus. Motion direction sensitivity (or motion sensitivity in general) was not observed in occipital or ventral temporal cortex.

Fig. 6.. MT+ resting-state connectivity.

When the time course from each subdivision of MT+ was used as a seed for resting-state correlations, functional connectivity with other subdivisions, including the opposite hemisphere and relatively consistent network of other regions was revealed (r > 0.4). In both hemispheres, ventral, but not dorsal, MT+ was correlated with the small portion of residual V1 in occipital cortex. Correlations with IPS were observed for both dorsal and ventral MT+ seeds though were stronger in the left hemisphere. Dashed, semi-transparent white circles denote seed region. Solid white circular outlines illustrate MT+ in the hemisphere opposite that of the seed.

Fig. 7.. Motion psychophysics results.

For high-contrast (98%+ contrast) random dot kinematograms (RDKs) with larger-than-typical dot sizes (2.85°), MC showed above-chance performance for (A) motion detection, (B) discrimination of motion translation, rotation and flow and (C) discrimination opposite directions of motion for translation and rotation (with mixed results for flow). (D) Moreover, for all categories of motion, her direction discrimination scaled with motion coherence (though results for flow were noisier). (E) MC was best able to detect gratings at low spatial and high temporal frequencies. MC showed a poorer ability to discriminate motion direction for (F) square-wave gratings than (G) single bar of the grating.

Fig. 8.. Psychophysical contrast response functions.

In a 2-alternative forced-choice decision, MC’s ability to detect a flickering checkerboard increased logarithmically within contrast.