Neural differentiation is moderated by age in scene- but not face-selective cortical regions

Abstract

<jats:title>Abstract</jats:title><jats:p>The aging brain is characterized by neural dedifferentiation – an apparent decrease in the functional selectivity of category-selective cortical regions. Age-related reductions in neural differentiation have been proposed to play a causal role in cognitive aging. Recent findings suggest, however, that age-related dedifferentiation is not equally evident for all stimulus categories and, additionally, that the relationship between neural differentiation and cognitive performance is not moderated by age. In light of these findings, in the present experiment younger and older human adults (males and females) underwent fMRI as they studied words paired with images of scenes or faces prior to a subsequent memory task. Neural selectivity was measured in two scene-selective (parahippocampal place area and retrosplenial cortex) and two face-selective (fusiform and occipital face areas) regions of interest using both a univariate differentiation index and multivoxel pattern similarity analysis. Both methods provided highly convergent results which revealed evidence of age-related reductions in neural dedifferentiation in scene-selective but not face-selective cortical regions. Additionally, neural differentiation in the parahippocampal place area demonstrated a positive, age-invariant relationship with subsequent source memory performance (recall of the image category paired with each recognized test word). These findings extend prior findings suggesting that age-related neural dedifferentiation is not a ubiquitous phenomenon, and that the specificity of neural responses to scenes is predictive subsequent memory performance independently of age.</jats:p><jats:sec><jats:title>Significance Statement</jats:title><jats:p>Increasing age is associated with reduced neural specificity in cortical regions that are selectively responsive to a given perceptual stimulus category (age-related neural dedifferentiation), a phenomenon which has been proposed to contribute to cognitive aging. Recent findings reveal that age-related neural dedifferentiation is not present for all types of visual stimulus categories, and the factors which determine when the phenomenon arises remain unclear. Here, we demonstrate that scene- but not face-selective cortical regions exhibit age-related neural dedifferentiation during an attentionally-demanding task. Additionally, we report that higher neural selectivity in the scene-selective ‘parahippocampal place area’ is associated with better memory performance after controlling for variance associated with age group, adding to evidence that neural differentiation impacts cognition across the adult lifespan.</jats:p></jats:sec>

Tracking Age Differences in Neural Distinctiveness across Representational Levels

“…In contrast to previous studies (e.g., Srokova et al, 2020), we did not observe differences in age-related neural dedifferentiation based on stimulus materials.…”

“…However, when tested by itself, category selectivity also showed to be related to memory performance across participants. The finding that category selectivity was associated with recognition performance while category specificity was not, was also observed by Srokova et al (2020). However, in contrast to that, report a link between recognition memory and both category selectivity and specificity.…”

“…The available evidence clearly supports the notion of age-related neural dedifferentiation of category information. Focusing on age differences in the representation of 6 broader categories such as faces, houses, or objects within the ventral visual cortex (VVC;Park et al, 2004Park et al, , 2012Payer et al, 2006;Srokova et al, 2020;Voss et al, 2008), previous studies made use of the preferential response of these regions to specific stimulus categories (Epstein and Kanwisher, 1998;Grill-Spector and Malach, 2004;Kanwisher et al, 1997). For example, using conventional univariate analyses, Park et al (2004) demonstrated that, compared to young adults, older adults exhibited less category-selective blood oxygen level dependent (BOLD) responses to stimuli of faces, houses, chairs, and pseudowords, providing the first human evidence for age-related neural dedifferentiation in the VVC (see also Park et al, 2012;Payer et al, 2006, and, accounting for trial-wise BOLD variability: Voss et al, 2008).…”

Tracking Age Differences in Neural Distinctiveness across Representational Levels

“…The available evidence clearly supports the notion of age-related neural dedifferentiation of category information. Focusing on age differences in the representation of broader categories such as faces, houses, or objects within the ventral visual cortex (VVC;Park et al, 2004Park et al, , 2012Payer et al, 2006;Srokova et al, 2020;Voss et al, 2008), previous studies made use of the preferential response of these regions to specific stimulus categories (Epstein and Kanwisher, 1998;Grill-Spector and Malach, 2004;Kanwisher et al, 1997). For example, using conventional univariate analyses, Park et al (2004) demonstrated that, compared to young adults, older adults exhibited less category-selective blood oxygen level dependent (BOLD) responses to stimuli of faces, houses, chairs, and pseudowords, providing the first human evidence for age-related neural dedifferentiation in the VVC (see also Park et al, 2012;Payer et al, 2006, and, accounting for trial-wise BOLD variability: Voss et al, 2008).…”

A Functional MRI Paradigm for Efficient Mapping of Memory Encoding Across Sensory Conditions

“…Within the visual condition, we chose to present faces and spatial scenes, motivated by work on face-selective and sceneselective brain regions (Kanwisher et al, 1997;Epstein and Kanwisher, 1998;Gazzaley et al, 2005;Collins and Dickerson, 2019). Further, those stimuli seemed to show differences in agerelated reductions in neural dedifferentiation, which makes them interesting for longitudinal studies (Srokova et al, 2020). To select auditory stimuli on a similar level of specificity, we chose voice and environmental stimuli motivated by previous work on voice-selective brain regions (Belin et al, 2000(Belin et al, , 2002Pernet et al, 2015;Agus et al, 2017;Zäske et al, 2017;Aglieri et al, 2018).…”