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Articles, Behavioral/Cognitive

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

Felicia W. Sun, Michael R. Stepanovic, Joseph Andreano, Lisa Feldman Barrett, Alexandra Touroutoglou and Bradford C. Dickerson
Journal of Neuroscience 14 September 2016, 36 (37) 9659-9668; DOI: https://doi.org/10.1523/JNEUROSCI.1492-16.2016
Felicia W. Sun
3Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02114, and
4Psychiatric Neuroimaging Division, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02114, and
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Michael R. Stepanovic
1Frontotemporal Disorders Unit, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02129,
2Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02114,
3Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02114, and
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Joseph Andreano
3Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02114, and
4Psychiatric Neuroimaging Division, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02114, and
5Department of Psychology, Northeastern University, Boston, Massachusetts 02115
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Lisa Feldman Barrett
3Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02114, and
4Psychiatric Neuroimaging Division, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02114, and
5Department of Psychology, Northeastern University, Boston, Massachusetts 02115
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Alexandra Touroutoglou
2Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02114,
3Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02114, and
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Bradford C. Dickerson
1Frontotemporal Disorders Unit, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02129,
2Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02114,
3Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02114, and
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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.

  • aging
  • cerebral cortex
  • default mode network
  • memory
  • salience network

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The Journal of Neuroscience: 36 (37)
Journal of Neuroscience
Vol. 36, Issue 37
14 Sep 2016
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Youthful Brains in Older Adults: Preserved Neuroanatomy in the Default Mode and Salience Networks Contributes to Youthful Memory in Superaging
Felicia W. Sun, Michael R. Stepanovic, Joseph Andreano, Lisa Feldman Barrett, Alexandra Touroutoglou, Bradford C. Dickerson
Journal of Neuroscience 14 September 2016, 36 (37) 9659-9668; DOI: 10.1523/JNEUROSCI.1492-16.2016

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Youthful Brains in Older Adults: Preserved Neuroanatomy in the Default Mode and Salience Networks Contributes to Youthful Memory in Superaging
Felicia W. Sun, Michael R. Stepanovic, Joseph Andreano, Lisa Feldman Barrett, Alexandra Touroutoglou, Bradford C. Dickerson
Journal of Neuroscience 14 September 2016, 36 (37) 9659-9668; DOI: 10.1523/JNEUROSCI.1492-16.2016
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Keywords

  • aging
  • cerebral cortex
  • default mode network
  • memory
  • salience network

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  • Anatomic concordance in cortical preserved areas in youthful and "fit" brains
    Fabio H. G. Porto
    Published on: 06 October 2016
  • Published on: (6 October 2016)
    Page navigation anchor for Anatomic concordance in cortical preserved areas in youthful and "fit" brains
    Anatomic concordance in cortical preserved areas in youthful and "fit" brains
    • Fabio H. G. Porto, MD
    • Other Contributors:
      • Artur M. N. Coutinho, Ricardo Nitrini, Carlos A. Buchpiguel, Sonia M. D. Brucki

    We read this paper with great interest. We considered of particular interest the results showing preservation of cortical thickness in specific regions that play a role as hubs of the salience and default mode networks in "superagers", in comparison with older adults with typical age-related expected decline in cognition.

    As physical activity is a well know protective factor against cognitive decline, it would...

    Show More

    We read this paper with great interest. We considered of particular interest the results showing preservation of cortical thickness in specific regions that play a role as hubs of the salience and default mode networks in "superagers", in comparison with older adults with typical age-related expected decline in cognition.

    As physical activity is a well know protective factor against cognitive decline, it would be interesting to know if any measure of aerobic fitness or exercise index (current or past) are at disposal to examine possible differences between those groups. We believe this would be particularly important considering our recently published data showing metabolic changes measured with FDG-PET in areas that correspond to hubs of both networks in subjects with mild cognitive impairment (MCI) after 24 weeks of aerobic training (Porto et al., 2015). Surprisingly, the areas with more important metabolic changes were the rostral anterior cingulate cortex (ACC) (decrease in resting-state metabolism) and the retrosplenial cortex (increase in resting-state metabolism). Also, physical activity decreased the intensity of the precuneus metabolic impairment in the MCI group in relation to a control group after the aerobic training. We hypothesized an increase in efficacy in the salience network induced by physical training (reflected by its decreased metabolism at rest) may influence the default mode network due to better regulation of brain networks, increasing the metabolism at rest in the precuneus, an important node of this network.

    A volumetric increase in the rostral ACC was already shown after an aerobic training program in cognitively normal older adults (Colcombe et al., 2006). Interestingly, while studying the acute effects of aerobic exercise in rest brain glucose metabolism in normal young adults, other authors found a generalized metabolic decrease in all investigated areas, particularly in the dorsal ACC (Kemppainen et al., 2005). When participants were split into two groups ("trained" versus "less trained"), the trained group had a noticeable reduction in the dorsal ACC when compared to the less trained group, suggesting some type of long-term adaptive metabolic changes in the region. This is concordant with our findings. As others studies of "superagers" have been showing preservation of the ACC (Harrison et al., 2012; Rogalski et al., 2012; Gefen et al., 2015), this node of the salience network may have an important role in the relationship between physical fitness and cognitive preservation.

    It is possible that neuroplasticity induced by long-term physical exercise may also influence the thickness of the cortex in "superagers", as there is an anatomical concordance between brain regions that changed after our (and others) aerobic program and those preserved in older adults with youthful memory. There might be an important link between both studies, eventually suggesting potential mechanisms between global health and the "superagers" cortical signature.

    A suggestion for future studies is to take into account measures of past and current physical fitness when comparing cognition, brain structure and function in different groups of older subjects, once it is possible that better fitness is related to healthier brain aging.

    References:

    Colcombe SJ, Erickson KI, Scalf PE, Kim JS, Prakash R, McAuley E, Elavsky S, Marquez DX, Hu L, Kramer AF (2006) Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci 61:1166-1170.

    Gefen T, Peterson M, Papastefan ST, Martersteck A, Whitney K, Rademaker A, Bigio EH, Weintraub S, Rogalski E, Mesulam M-MM, Geula C (2015) Morphometric and histologic substrates of cingulate integrity in elders with exceptional memory capacity. J Neurosci 35:1781-1791.

    Harrison TM, Weintraub S, Mesulam MM, Rogalski E (2012) Superior memory and higher cortical volumes in unusually successful cognitive aging. J Int Neuropsychol Soc 18:1081-1085.

    Kemppainen J, Aalto S, Fujimoto T, Kalliokoski KK, L?ngsj? J, Oikonen V, Rinne J, Nuutila P, Knuuti J (2005) High intensity exercise decreases global brain glucose uptake in humans. J Physiology 568:323-332.

    Porto FH, Coutinho AM, Pinto AL, Gualano B, Duran FL, Prando S, Ono CR, Sp?ndola L, Oliveira MO, Vale PH, Nitrini R, Buchpiguel CA, Brucki SM (2015) Effects of Aerobic Training on Cognition and Brain Glucose Metabolism in Subjects with Mild Cognitive Impairment. J Alzheimer's Dis 46:747-760.

    Rogalski EJ, Gefen T, Shi J, Samimi M, Bigio E, Weintraub S, Geula C, Mesulam MM (2012) Youthful Memory Capacity in Old Brains: Anatomic and Genetic Clues from the Northwestern SuperAging Project. J Cognitive Neurosci 25:29-36.

    Sun FW, Stepanovic MR, Andreano J, Barrett LF, Touroutoglou A, Dickerson BC (2016) Youthful Brains in Older Adults: Preserved Neuroanatomy in the Default Mode and Salience Networks Contributes to Youthful Memory in Superaging. J Neurosci 36:9659-9668.

    Conflict of Interest:

    None declared

    Show Less
    Competing Interests: None declared.

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