Youthful Brains in Older Adults: Preserved Neuroanatomy in the Default Mode and Salience Networks Contributes to Youthful Memory in Superaging - PubMed (original) (raw)

Youthful Brains in Older Adults: Preserved Neuroanatomy in the Default Mode and Salience Networks Contributes to Youthful Memory in Superaging

Felicia W Sun et al. J Neurosci. 2016.

Abstract

Decline in cognitive skills, especially in memory, is often viewed as part of "normal" aging. Yet some individuals "age better" than others. Building on prior research showing that cortical thickness in one brain region, the anterior midcingulate cortex, is preserved in older adults with memory performance abilities equal to or better than those of people 20-30 years younger (i.e., "superagers"), we examined the structural integrity of two large-scale intrinsic brain networks in superaging: the default mode network, typically engaged during memory encoding and retrieval tasks, and the salience network, typically engaged during attention, motivation, and executive function tasks. We predicted that superagers would have preserved cortical thickness in critical nodes in these networks. We defined superagers (60-80 years old) based on their performance compared to young adults (18-32 years old) on the California Verbal Learning Test Long Delay Free Recall test. We found regions within the networks of interest where the cerebral cortex of superagers was thicker than that of typical older adults, and where superagers were anatomically indistinguishable from young adults; hippocampal volume was also preserved in superagers. Within the full group of older adults, thickness of a number of regions, including the anterior temporal cortex, rostral medial prefrontal cortex, and anterior midcingulate cortex, correlated with memory performance, as did the volume of the hippocampus. These results indicate older adults with youthful memory abilities have youthful brain regions in key paralimbic and limbic nodes of the default mode and salience networks that support attentional, executive, and mnemonic processes subserving memory function.

Significance statement: Memory performance typically declines with age, as does cortical structural integrity, yet some older adults maintain youthful memory. We tested the hypothesis that superagers (older individuals with youthful memory performance) would exhibit preserved neuroanatomy in key brain networks subserving memory. We found that superagers not only perform similarly to young adults on memory testing, they also do not show the typical patterns of brain atrophy in certain regions. These regions are contained largely within two major intrinsic brain networks: the default mode network, implicated in memory encoding, storage, and retrieval, and the salience network, associated with attention and executive processes involved in encoding and retrieval. Preserved neuroanatomical integrity in these networks is associated with better memory performance among older adults.

Keywords: aging; cerebral cortex; default mode network; memory; salience network.

Copyright © 2016 Sun, Stepanovic et al.

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Figures

Figure 1.

Figure 1.

We used a network approach to test the hypothesis that preserved memory in superaging is associated with preserved structure in the salience network and default mode network. We used masks of the salience network (blue) anchored in the dorsal anterior insula (Touroutoglou et al., 2012) and the default mode network (yellow; Andrews-Hanna et al., 2010) in our primary analyses of preserved brain structure in superaging. For the binarized salience network, z < 0.2, and for the default mode network, z < 0.2 (maps are shown on the “fsaverage” subject's inflated cortical surface). The general linear model analysis depicted in Figure 2 focuses only on cortex within these two networks.

Figure 2.

Figure 2.

Regions of preserved cortical thickness in superagers within the default mode and salience networks. A, This statistical map shows regions where the cortex of superagers is thicker than in typical older adults (p < 0.05; depicted as a red-to-yellow heat gradient), highlighting regions within a priori hypothesized networks of interest (salience network in blue; default mode network in pale yellow). Four control regions in primary sensory cortical areas outside the networks of interest are labeled for comparison. B, Bar graphs show mean cortical thickness within each region labeled in the map. Although by definition all of these regions are thicker in superagers than typical older adults (TOAs), some of them are thinner in superagers than in young adults (partial preservation indicated with asterisks), while all others are “youthful” in superagers (fully preserved cortical thickness relative to young adults). R, Right hemisphere; L, left hemisphere. Error bars indicate SE.

Figure 3.

Figure 3.

Preserved cortical thickness in some regions within default mode and salience networks supports preserved memory in elderly adults. The brain maps adjacent to scatter plots show regions where the cortex of superagers is thicker than in typical older adults (p < 0.05; depicted as solid white), highlighting the hypothesized networks of interest (salience network in blue; default mode network in pale yellow). Scatterplots in A and B illustrate the correlation between memory performance in the entire older adult group (superagers indicated by hollow points) and adjusted cortical thickness (standardized residuals after regressing out global mean cortical thickness, plus a constant) in the rostral medial prefrontal (A; r = 0.45, p < 0.01) and the midcingulate cortex (B; r = 0.55, p < 0.001). The scatterplot in C shows no such relationship between memory performance and cortical thickness within one of the sensory regions used as a control.

Figure 4.

Figure 4.

Preserved hippocampal volume—a key node in the default mode network—correlates with preserved memory in elderly adults. A, Larger total hippocampal volume (sum of left and right hemispheres divided by total intracranial volume; as depicted, multiplied by a constant) is correlated with better episodic memory performance in the entire group of older adults (superagers indicated by hollow points). B, Parasagittal T1-weighted MRI scans at the level of the long axis of the hippocampus illustrate the effect shown in the scatterplot by showing the individuals with the largest (green) and smallest (red) hippocampal volume within the entire older adult sample. The individual with the largest hippocampal volume (green) is an 81-year-old male, has 20 years of education, and was able to freely recall 15 of the 16 words on the CVLT after the long delay. The individual with the smallest hippocampal volume (red) is a 74-year-old male, has 16 years of education, and was able to freely recall 9 of the 16 words on the CVLT after the long delay.

Figure 5.

Figure 5.

Superaging signature. The figure shows key nodes of the salience network (blue) and default mode network (yellow) where superagers and young adults are indistinguishable in cortical thickness. Preserved thickness in these regions is what distinguishes superagers from typical older adults.

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