Pupillary responses and memory-guided visual search reveal age-related and Alzheimer’s-related memory decline

Abstract

Episodic memory - composed of memory for unique spatiotemporal experiences - is known to decline with aging, and even more severely in Alzheimer 's disease (AD). Memory for trial-unique objects in spatial scenes depends on the integrity of the hippocampus and interconnected structures that are among the first areas affected in AD. We reasoned that memory for objects-in-scenes would be impaired with aging, and that further impairments would be observed in AD. We asked younger adults, healthy older adults, older adults at-risk for developing cognitive impairments, and older adults with probable early AD to find changing items ('targets') within images of natural scenes, measuring repeated-trial changes in search efficiency and pupil diameter. Compared to younger adults, older adults took longer to detect target objects in repeated scenes, they required more fixations and those fixations were more dispersed. Whereas individuals with AD showed some benefit of memory in this task, they had substantially longer detection times, and more numerous, dispersed fixations on repeated scenes compared to age-matched older adults. Correspondingly, pupillary responses to novel and repeated scenes were diminished with aging and further in AD, and the memory-related changes were weaker with aging and absent in AD. Our results suggest that several nonverbal measures from memory-guided visual search tasks can index aging and Alzheimer's disease status, including pupillary dynamics. The task measurements are sensitive to the integrity of brain structures that are associated with Alzheimer's-related neurodegeneration, the task is well tolerated across a range of abilities, and thus, it may prove useful in early diagnostics and longitudinal tracking of memory decline.

Hippocampal gamma‐band Synchrony and pupillary responses index memory during visual search

“…These findings are generally consistent with previous work on search efficiency and contextual cueing with scene/array repetition (Chun and Jiang, 1998;Peterson and Kramer, 2001;Chun and Jiang, 2003;Tseng and Li, 2004;Brockmole and Henderson, 2006;Wynn et al, 2016). Additionally, macaques showed pupil dilation with scene repetition, consistent with recognition memory in humans (Naber et al, 2013;Dragan et al, 2016). To ensure sufficient data samples during search, we removed the trials with prohibitively rapid detection times, comprising 4% of Novel trials and 14% of repeated trials, see Figure 4c.…”

Cognitive workload across the spectrum of cognitive impairments: A systematic review of physiological measures

“…This may be reflected by reduced functional connectivity (Hata et al, 2016), decreased pupillary responses (Dragan et al, 2017) or alterations of pupil's light reflex (Bittner et al, 2014). Patients with AD showed greater cognitive workload accompanied with decreased behavioral performances during the cognitive task compared to older adults with MCI or healthy older adults (Leyhe et al, 2009;Saur et al, 2010;Sole-Padulles et al, 2009;van der Hiele et al, 2007;van Deursen et al, 2011;van Deursen et al, 2008).…”

“…Few studies were performed with cardiovascular measures or pupillometry. One of the reasons could be due to medication intake or physiological changes related to aging that limit the sensitivity of these techniques (Allard et al, 2010;Bittner et al, 2014;Dragan et al, 2017;Ennis et al, 2013;Hess & Ennis, 2012). Contrary to fMRI or PET measures, cardiovascular and pupillary measures provide no clues about the locations of the underlying controlling neural systems.…”

“…This result suggests that older adults needed a greater effort than younger adults to reach their level of success. Dragan et al (2017) examined the relationship between memory-guided visual search and pupillary responses in different groups of adults including one group of younger adults and one group of healthy older adults. Two memory tasks were administered in which participants had to detect the target in a visual scene.…”

“…d. Pupillometry Dragan et al (2017) examined the relationship between memory-guided visual search and pupillary responses in patients with MCI, patients with AD, and healthy older adults, using two memory tasks. Findings showed that patients with probable early AD had worse memory-guided search than healthy older adults.…”