Altered visual and haptic verticality perception in posterior cortical atrophy and Alzheimer's disease

• Published in: The Journal of physiology Vol. 600; no. 2; pp. 373 - 391
• Main Authors: Day, Brian L., Ocal, Dilek, Peters, Amy, Bancroft, Matthew J., Cash, David, Kaski, Diego, Crutch, Sebastian J., Yong, Keir X. X.
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 01.01.2022
• Subjects: Alzheimer Disease; Alzheimer's disease; Atrophy; Bias; Cortex (parietal); Dementia disorders; gravity; Haptic Technology; Haptics; Humans; Neurodegenerative diseases; Orientation behavior; posterior cortical atrophy; Posture; Somatosensory cortex; Space Perception; spatial orientation; verticality perception; Visual Perception; Visual stimuli; verticality perception; posterior cortical atrophy; spatial orientation; Alzheimer's disease; gravity
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/JP282289

There is increasing theoretical and empirical support for the brain combining multisensory information to determine the direction of gravity and hence uprightness. A fundamental part of the process is the spatial transformation of sensory signals between reference frames: eye‐centred, head‐centred, body‐centred, etc. The question ‘Am I the right way up?’ posed by a patient with posterior cortical atrophy (PCA) suggests disturbances in upright perception, subsequently investigated in PCA and typical Alzheimer's disease (tAD) based on what looks or feels upright. Participants repeatedly aligned to vertical a rod presented either visually (visual‐vertical) or haptically (haptic‐vertical). Visual‐vertical involved orienting a projected rod presented without or with a visual orientation cue (circle, tilted square (±18°)). Haptic‐vertical involved orientating a grasped rod with eyes closed using a combination of side (left, right) and hand (unimanual, bimanual) configurations. Intraindividual uncertainty and bias defined verticality perception. Uncertainty was consistently greater in both patient groups than in control groups, and greater in PCA than tAD. Bias in the frontal plane was strongly directionally affected by visual cue tilt (visual‐vertical) and grip side (haptic‐vertical). A model was developed that assumed verticality information from multiple sources is combined in a statistically optimal way to produce observed uncertainties and biases. Model results suggest the mechanism that spatially transforms graviceptive information between body parts is disturbed in both patient groups. Despite visual dysfunction being typically considered the primary feature of PCA, disturbances were greater in PCA than tAD particularly for haptic‐vertical, and are considered in light of posterior parietal vulnerability. Key points The perception of upright requires accurate and precise estimates of orientation based on multiple noisy sensory signals. The question ‘Am I the right way up?’ posed by a patient with posterior cortical atrophy (PCA; purported ‘visual variant Alzheimer's’) suggests disturbances in the perception of upright. What looks or feels upright in PCA and typical Alzheimer's disease (tAD) was investigated by asking participants to repeatedly align to vertical a rod presented visually (visual‐vertical) or haptically (haptic‐vertical). PCA and tAD groups exhibited not only greater perceptual uncertainty than controls, but also exaggerated bias induced by tilted visual orientation cues (visual‐vertical) and grip side (haptic‐vertical). When modelled, these abnormalities, which were particularly evident in PCA haptic‐vertical performance, were compatible with disruption of a mechanism that spatially transforms verticality information between body parts. The findings suggest an important role of posterior parietal cortex in verticality perception, and have implications for understanding spatial disorientation in dementia. figure legend Participants with posterior cortical atrophy (PCA), typical Alzheimer's disease (tAD) or controls (CON) repeatedly aligned to vertical a rod presented visually (visual‐vertical, top) or haptically in the absence of visual feedback (haptic‐vertical, bottom). For all tasks, participants’ subjective verticality estimation (SV) was defined by observed perceptual bias (mean) and uncertainty (SD). A mechanistic model was developed based on principles of maximum likelihood estimation (Gaussians, centre) to estimate the uncertainty (σ) associated with a primary mechanism which spatially transforms information from a system of graviceptors using information about whole‐body configuration (I, left). SV was modelled as the product of the primary mechanism (I) and independent local secondary mechanisms (II; retinal‐based or hand‐based for visual and haptic tasks, respectively). Conservative estimates of primary‐mechanism uncertainty (σ) were greatest in PCA relative to tAD and control groups across tasks (right; estimated means and 95% CI), being particularly apparent for the haptic‐vertical task.