Approaching objects cause confusion in patients with Alzheimer's disease regarding their direction of self-movement

Abstract

Navigation requires real-time heading estimation based-on self-movement cues from optic flow and object motion. We presented a simulated heading discrimination task to young, middle-aged and older adult, normal, control subjects and to patients with mild cognitive impairment or Alzheimer's disease. Age-related decline and neurodegenerative disease effects were evident on a battery of neuropsychological and visual motion psychophysical measures. All subject groups made more accurate heading judgements when using optic flow patterns than when using simulated movement past earth-fixed objects. When both optic flow and congruent object were presented together, heading judgements showed intermediate accuracy. In separate trials, we combined optic flow with non-congruent object motion, simulating an independently moving object. In the case of non-congruent objects, almost all of our subjects shifted their perceived self-movement to heading in the direction of the moving object. However, patients with Alzheimer's disease uniquely indicated that perceived self-movement was straight-ahead, in the direction of visual fixation. The tendency to be confused by objects that appear to move independently in the simulated visual scene corresponded to the difficulty patients with Alzheimer's disease encountered in real-world navigation through the hospital lobby (R(2) = 0.87). This was not the case in older normal controls (R(2) = 0.09). We conclude that perceptual factors limit safe, autonomous navigation in early Alzheimer's disease. In particular, the presence of independently moving objects in naturalistic environments limits the capacity of patients with Alzheimer's disease to judge their heading of self-movement.

Figure 1

Visual motion stimuli used in the cue conflict heading discrimination tasks. (A) Outward radial optic flow having a 30° left or right sided focus of expansion was formed by a randomly distributed pattern of white dots presented on a black background. A selected percentage of the dots were drawn from the pattern to undergo randomly directed motion to alter the strength of the simulated heading direction cue. The parameter estimation (PEST) algorithm controlled the percentage of randomly moving dots to determine each subject’s motion coherence thresholds. (B) Looming object motion simulated a filing cabinet viewed during the observer’s straight line path of approaching self-movement. The percentage of the full path length presented was selected to alter simulated heading direction signal strength and determine each subject’s path length thresholds. (C) Optic flow and object motion stimuli were superimposed to create two conditions with respect to a moving observer: Two cues simulating the same heading direction in congruent combination (left) as with an earth-fixed object. Two cues simulating different heading directions in incongruent combination (right) as with an independently moving animate object. (D) Top-down diagrammatic representation of the 24 incongruent stimulus conditions tested by combining four optic flow headings (±10° and ±20°) with six relative object motion headings (±5°, ±10° and ±15°).

Figure 2

Perceptual thresholds obtained in our four subject groups using optic flow and object motion stimuli. (A) Optic flow evoked similar motion coherence thresholds in younger, middle-aged and older normal controls subjects; whereas patients with early Alzheimer’s disease had thresholds that were roughly double those of the other groups. Object motion evoked steadily increasing path length thresholds across the four groups, the lowest thresholds in younger normal control subjects and the highest in patients with early Alzheimer’s disease. (B) Optic flow and object motion evoked perceptual thresholds were also obtained with the addition of heading direction jitter as frame-by-frame variation in the simulated heading direction. Heading jitter had a negligible effect on optic flow thresholds in all groups, but a substantial impact on object motion thresholds. Jitter effects on object motion threshold effects were larger in younger subjects and proportionately smaller in the older groups. YNC = younger normal controls; MNC = middle-aged normal controls; ONC = older normal controls; EAD = early Alzheimer’s disease. *indicates P < 0.05.

Figure 3

The effects of incongruent object motion on heading estimate errors relative to the heading direction simulated in optic flow having a ±10° heading (A) or ±20° heading (B) as recorded in five subject groups. All subject groups showed more lateral deflections of their perceived heading with more lateral object motion headings and more medial deflections with more medial object motion headings. All groups also showed a bias toward underestimating heading eccentricity that tended to be more substantial in older normal controls and MCI subjects and was more clearly seen in patients with in early Alzheimer’s disease. YNC = younger normal controls; MNC = middle-aged normal controls; ONC = older normal controls; EAD = early Alzheimer’s disease.

Figure 4

Heading estimation across five cue configurations and four subject groups. Heading estimation accuracy was determined by varying the simulated heading direction along the horizontal meridian in optic flow and object motion stimuli. Four optic flow or object motion headings were presented alone (±5°, ±10°, ±15°, ±20°, ±25°) or in a limited set of combination stimuli in which optic flow (±10° or ±20°) was combined with object motion either with matched headings (congruently superimposed) or with object motion heading displaced from the optic flow headings by ±5°, ±10° or ±15° (laterally or medially incongruently superimposed relative to the heading in optic flow). (A and B) Black and white bars depict results from optic flow and object motion alone or in congruent superimposition (Mapstone et al., 2006), included for comparison to results from incongruently superimposed cues (blue and red bars). Heading discrimination was most accurate using the optic flow stimuli alone compared to the object alone in all groups. Congruently combined optic flow and (simulated earth-fixed) objects allowed for heading discrimination which tended to be intermediate between the two single stimuli in all groups. With incongruent stimuli (simulating an independently moving object with respect to a moving observer) all normal control groups showed relatively uniform bias towards the object when it was more lateral to the simulated observer heading in optic flow. In contrast, the Alzheimer’s disease group did not show a bias toward the lateral object, but indicated self-movement heading was generally straight ahead in the direction of central visual fixation. On the other hand, a simulated object with a more medial heading than the observers’ simulated heading also led to bias toward the object, but with a pronounced ageing and disease effect Alzheimer’s disease > older normal controls > middle-aged normal controls > younger normal controls. YNC = younger normal controls; MNC = middle-aged normal controls; ONC = older normal controls; EAD = early Alzheimer’s disease.

Figure 5

Relationships between navigational performance and perceptual processing of self-movement cues. (A) Navigational performance was assessed in a real world navigational test battery implemented in the Strong Memorial Hospital lobby. Subjects were moved along a path (arrows) through the test environment and then presented with an 80 item test about the route and the environment. (B) Ageing and Alzheimer’s disease are linked to successive declines of navigational performance (ordinate, mean ± SEM). (C) Navigational test scores were not related to perceptual measures in younger groups, were weakly so in normal ageing but significantly so in patients with Alzheimer’s disease. Perceptual predictors of navigational performance included heading estimation with object motion alone and congruent optic flow and object. YNC = younger normal controls; MNC = middle-aged normal controls; ONC = older normal controls; EAD = early Alzheimer’s disease.