An expectation-based memory deficit in aging

Abstract

Memory performance can be enhanced by expectations regarding the appearance of ensuing stimuli. Here, we investigated the influence of stimulus-category expectation on memory performance in aging, and used fMRI to explore age-related alterations in associated neural mechanisms. Unlike younger adults, who demonstrated both working memory (WM) and long-term memory (LTM) performance benefits for face stimuli when this stimulus category was expected, older adults did not exhibit these memory benefits. Concordantly, older adults did not exhibit expectation-period activity modulation in visual association cortex (i.e., fusiform face area (FFA)), unlike younger adults. However, within the older population, individuals who demonstrated face-expectation memory benefits also exhibited expectation-period FFA activity modulation equivalent to younger adults. The older cohort also displayed diminished expectation-related functional connectivity between regions of the prefrontal cortex and the FFA, relative to younger adults, suggesting that network alterations underlie the absence of expectation-mediated cortical modulation and memory benefits. This deficit may have broader consequences for the effective utilization of predictive cues to guide attention and engender optimal cognitive performance in older individuals.

Figure 1. Experimental Paradigm

All participants performed 4 tasks (Stimulus-Known Faces (SKf trials), Stimulus-Known Scenes (SKs trials), Stimulus Unknown (SUf and SUs trials), and Passive View (PVf and PVs trials)), which were blocked and counterbalanced and stimuli were randomized. For Passive View trials, delay and probe periods were removed (see methods). Note that fixation crosses were green, red, and grey for expectation, delay, and inter-trial interval (ITI) periods, respectively (not shown in figure). SKf, stimulus-known face trials; SKs, stimulus-known scene trials; SUf, stimulus-unknown face trials; SUs, stimulus-unknown scene trials; PVf, passive-view face trials; PVs, passive-view scene trials.

Figure 2. Behavioral Performance. Younger vs. Older Adults

(A) WM Accuracy. Compared to neutrally cued stimuli (SUf & SUs), younger adults were significantly more accurate for predictively cued faces (SKf) (*p < 0.05) but not scenes (SKs) (p > 0.05). Older adults performed equivalently for predictively and neutrally cued faces (p > 0.05), as well as predictively and neutrally cued scene stimuli (p > 0.05). (B) LTM Performance. Compared to neutrally cued stimuli, younger adults remembered predictively cued faces better (*p < 0.05) but not scenes (p > 0.05). Older adults equivalently remembered predictively and neutrally cued faces (p > 0.05) and scene stimuli (p > 0.05). SKf, stimulus-known face trials; SKs, stimulus-known scene trials; SUf, stimulus-unknown face trials; SUs, stimulus-unknown scene trials; WM, working memory; LTM, long-term memory.

Figure 3. Expectation-period FFA/PPA Activity: Younger vs. Older Adults

(A) FFA Activity. In younger adults, expectation-related FFA activity (i.e., baseline shift) was greater for predictively (SKf) than for neutrally cued face trials (SUf) (*p < 0.05), while in older adults expectation-related FFA activity was equivalent for both predictively and neutrally cued face trials (p > 0.05). (B) PPA Activity. In younger and older adults, PPA activity was equivalent for both predictively (SKs) and neutrally (SUs) cued scene stimuli (p values > 0.05). FFA, fusiform face area; PPA, parahippocampal place area; SKf, stimulus-known face trials; SKs, stimulus-known scene trials; SUf, stimulus-unknown face trials; SUs, stimulus-unknown scene trials.

Figure 4. FFA Functional Connectivity: SKf > SUf

Older- versus younger-group expectation-related FFA connectivity contrast SKf > SUf. Axial slices and surface renderings illustrate FFA-seed functional connectivity group contrasts. This analysis revealed greater FFA-connectivity in the younger group for multiple frontal regions, including bilateral MFG (arrows 1 & 2), right dorsal SMG (arrow 3), right IFJ (arrow 4), and right inferior frontal gyrus, as well basal ganglia - left nucleus accumbens, caudate, putamen and right pallidum, putamen. Four regions showed predictive-cue related connectivity increases in older adults: left intracalcarine cortex, left planum temporale, PCC, and retrosplenial cortex. FFA, fusiform face area; MFG, middle frontal gyrus; SMG, supramarginal gyrus; IFJ, inferior frontal junction; PCC, posterior cingulate cortex; SKf, stimulus-known face condition; SUf, stimulus-unknown face condition; PVf, passive-view face condition.