Temporal Integration of 3D Coherent Motion Cues Defining Visual Objects of Unknown Orientation is Impaired in Amnestic Mild Cognitive Impairment and Alzheimer's Disease

Abstract

The nature of visual impairments in Alzheimer's disease (AD) and their relation with other cognitive deficits remains highly debated. We asked whether independent visual deficits are present in AD and amnestic forms of mild cognitive impairment (MCI) in the absence of other comorbidities by performing a hierarchical analysis of low-level and high-level visual function in MCI and AD. Since parietal structures are a frequent pathophysiological target in AD and subserve 3D vision driven by motion cues, we hypothesized that the parietal visual dorsal stream function is predominantly affected in these conditions. We used a novel 3D task combining three critical variables to challenge parietal function: 3D motion coherence of objects of unknown orientation, with constrained temporal integration of these cues. Groups of amnestic MCI (n = 20), AD (n = 19), and matched controls (n = 20) were studied. Low-level visual function was assessed using psychophysical contrast sensitivity tests probing the magnocellular, parvocellular, and koniocellular pathways. We probed visual ventral stream function using the Benton Face Recognition task. We have found hierarchical visual impairment in AD, independently of neuropsychological deficits, in particular in the novel parietal 3D task, which was selectively affected in MCI. Integration of local motion cues into 3D objects was specifically and most strongly impaired in AD and MCI, especially when 3D motion was unpredictable, with variable orientation and short-lived in space and time. In sum, specific early dorsal stream visual impairment occurs independently of ventral stream, low-level visual and neuropsychological deficits, in amnestic types of MCI and AD.

Aging of Low and High Level Vision: From Chromatic and Achromatic Contrast Sensitivity to Local and 3D Object Motion Perception

“…This was an important finding because this accelerated high-level deterioration has remained hitherto unreported. This is one of the main novelties of the paper, extending our own previous use of this paradigm in normal elderly and pathological aging populations [3], [36].…”

“…It is well known that 3D tasks (requiring the detection of complex SFM targets) involve high-level dorsal stream function and dorso-ventral integration for object recognition [3], [36]. On the other hand, local speed signals are mainly processed in early human visual cortex, in particular V1 and V2 [41].…”

“…This task was very easy to perform because the “sphere” becomes very noticeable, with a strong 3D percept, once stimuli are above threshold [36]. Comprehension and performance can be controlled by analyzing the shape of the curve of the psychophysical staircase (if the subjects understand the task, the staircase converges in a monotonic way to asymptotic threshold levels).…”

“…Finally we addressed high-level motion integration and object perception using a 3D task (Structure from Motion, SFM) requiring high-level motion coherence [34], [35], [36], [37]. This task targets dorsal stream function and dorso-ventral integration for object recognition [3], [36].…”

Opposing effects of glutamatergic and GABAergic pharmacological manipulations on a visual perception task with relevance to schizophrenia

“…For instance, Alzheimer's has been associated with changes in light contrast sensitivity and 3D coherent motion (Kirby et al 2010;Lemos et al 2012;Risacher et al 2013), autism spectrum disorder (ASD) with changes in perceptual grouping and coherent motion (Farran and Brosnan 2011;Robertson et al 2014;Scherf et al 2008), and schizophrenia with visual hallucinations and differences in contour integration . Surprisingly, these differences and the potential contribution of these differences to symptom severity have remained largely unexplored.…”