Nutritional Neuroscience An International Journal on Nutrition, Diet and Nervous System ISSN: 1028-415X (Print) 1476-8305 (Online) Journal homepage: http://www.tandfonline.com/loi/ynns20 Determinants of fluid intelligence in healthy aging: Omega-3 polyunsaturated fatty acid status and frontoparietal cortex structure Marta K. Zamroziewicz, Erick J. Paul, Chris E. Zwilling & Aron K. Barbey To cite this article: Marta K. Zamroziewicz, Erick J. Paul, Chris E. Zwilling & Aron K. Barbey (2017): Determinants of fluid intelligence in healthy aging: Omega-3 polyunsaturated fatty acid status and frontoparietal cortex structure, Nutritional Neuroscience, DOI: 10.1080/1028415X.2017.1324357 To link to this article: http://dx.doi.org/10.1080/1028415X.2017.1324357 Published online: 11 May 2017. Submit your article to this journal Article views: 1708 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ynns20 Download by: [179.179.188.14] Date: 16 June 2017, At: 19:25 Determinants of fluid intelligence in healthy aging: Omega-3 polyunsaturated fatty acid status and frontoparietal cortex structure Marta K. Zamroziewicz 1,2,3, Erick J. Paul1,2, Chris E. Zwilling 1,2, Aron K. Barbey 1,2,3,4,5,6,7 1Decision Neuroscience Laboratory, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA, 2Beckman Institute for Advanced Science and Technology, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA, 3Neuroscience Program, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA, 4Department of Psychology, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA, 5Carle Neuroscience Institute, Carle Foundation Hospital, Urbana, IL 61801, USA, 6Department of Internal Medicine, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA, 7Institute for Genomic Biology, University of Illinois Urbana- Champaign, Champaign, IL 61801, USA Introduction: Accumulating evidence indicates that cognitive decline depends not only upon changes in brain health, but critically, also upon nutritional status. Decline in fluid intelligence, one of the most debilitating aspects of cognitive aging, has been linked to omega-3 polyunsaturated fatty acid (PUFA) status; however, it is not known whether this phenomenon results from specific omega-3 PUFAs acting on particular aspects of brain health. Therefore, this study aims to explore whether particular patterns of omega-3 PUFAs influence fluid intelligence by supporting specific neural structures. Methods: We measured six plasma phospholipid omega-3 PUFAs, fluid intelligence, and regional gray matter volume in the frontal and parietal cortices in 100 cognitively intact older adults (65–75 years old). A four-step mediation analysis was implemented using principal component analysis and multivariate linear regressions, adjusted for age, gender, education, and body mass index. Results: The mediation analysis revealed that one pattern of omega-3 PUFAs, consisting of alpha-linolenic acid, stearidonic acid, and eicosatrienoic acid, was linked to fluid intelligence, and that total gray matter volume of the left frontoparietal cortex (FPC) fully mediated the relationship between this omega-3 PUFA pattern and fluid intelligence. Discussion: These data demonstrate that fluid intelligence may be optimally supported by specific omega-3 PUFAs through preservation of FPC gray matter structure in cognitively intact older adults. This report provides novel evidence for the benefits of particular omega-3 PUFA patterns on fluid intelligence and underlying gray matter structure. Keywords: Nutrient biomarkers, Nutrient biomarker patterns, Cognitive performance, Cognitive aging, Cortical integrity, Brain aging, Nutritional cognitive neuroscience Introduction growth in the proportion of older adults, the search Nutrition has increasingly been recognized for its for effective strategies to promote healthy brain ability to help prevent and protect against disease, aging provides a catalyst for research to investigate and at the frontiers of this effort is research within the beneficial effects of nutrition on the aging brain. the emerging interdisciplinary field of Nutritional In the absence of neurodegenerative disease, decline Cognitive Neuroscience. This line of work demon- in fluid intelligence presents as one of the most debil- strates that cognitive decline depends not only upon itating aspects of cognitive aging.2 Fluid intelligence changes in brain structure and brain function, but cri- refers to the intellectual abilities required for adaptive tically, also upon dietary intake and nutritional problem solving in novel situations, and reflects the status.1 As the United States experiences rapid capacity to creatively and flexibly grapple with the world in ways that do not rely on prior knowledge.3 Correspondence to: Aron K. Barbey, Decision Neuroscience Laboratory, A fundamental issue in the study of cognitive aging Beckman Institute for Advanced Science and Technology, University of has historically been whether fluid intelligence can Illinois, Urbana, IL 61801, USA. 4 Email: [email protected]; http://DecisionNeuroscienceLab.org/ be maintained in late adulthood. Indeed, recent ©2017InformaUKLimited,tradingasTaylor&FrancisGroup DOI 10.1080/1028415X.2017.1324357 Nutritional Neuroscience 2017 1 Zamroziewicz et al. Determinants of fluid intelligence in healthy aging evidence indicates that age-related decline in fluid cognitive training or dietary intervention studies, and intelligence is mediated by nervous system health, contraindications for magnetic resonance imaging highlighting the potential for intervention by neuro- (MRI). All participants were right handed with protective nutrients.5 normal, or corrected to normal vision and no contra- Increasing evidence suggests that omega-3 (n-3) indication for MRI. Of these 122 participants, 22 par- polyunsaturated fatty acids (PUFAs) benefit the ticipants did not have a complete dataset, which aging brain.6 PUFAs are known to contribute to included neuropsychological testing, MRI, and structural integrity of neuronal membranes, control blood biomarker analysis. Therefore, 100 participants inflammation and oxidation, and promote energy were considered in the current analysis. metabolism.7 Omega-3 PUFAs have been linked to the preservation of cognitive functions vulnerable to Standard protocol approval and participant age-related decline, including fluid intelligence.8 consent However, it is not known which brain structures n-3 This study was approved by the University of Illinois PUFAs may act upon to support fluid intelligence, Institutional Review Board and the Carle Hospital and whether particular patterns of n-3 PUFAs prefer- Institutional Review Board and, in accordance with entially provide support. the stated guidelines, all participants read and signed Fluid intelligence engages a distributed brain circuit informed consent documents. within the frontal and parietal cortex.9,10 Specifically, fluid intelligence is linked to structural integrity and Biomarker acquisition and analysis neural activity within the lateral prefrontal and Plasma lipids were extracted by the method of Folch posterior parietal cortices, regions cumulatively et al.16 Briefly, the internal standard (25 μgeachof referred to as the frontoparietal cortex (FPC).11,12 PC17:0) was added to 200 μl of serum, followed by Importantly, n-3 PUFAs slow age-related structural 6 ml of choloroform:methanol:BHT (2:1:100 v/v/w). decline in the FPC,13,14 and in this way, could The protein precipitate was removed by centrifugation prevent age-related decline in fluid intelligence. Thus, (2500 g, 5 minutes, 4°C). Then 1.5 ml of 0.88% KCl the FPC plays a critical role in fluid intelligence and was added to the supernatant, shaken vigorously and is amenable to n-3 PUFAs, making it a target region the layers were allowed to settle for 5 minutes. The of interest for investigating the impact of n-3 PUFAs upper layer was discarded and 1 ml of distilled water: on the cognitive and neural mechanisms of fluid methanol (1:1 v/v) was added, the tube was shaken intelligence. again and the layers were allowed to settle for 15 In summary, one of the most debilitating aspects of minutes. The lower layer was transferred into a clean cognitive aging, decline in fluid intelligence and tube and evaporated to dryness under nitrogen. The degeneration of the underlying FPC, may be amelio- phospholipid subfraction was separated by solid- rated by n-3 PUFA intake. However, it is not known phase extraction using aminopropyl columns, as whether particular patterns of n-3 PUFAs influence described by Aryen et al.17 Then the phospholipid core brain regions to support fluid intelligence. fraction was methylated by adding 2 ml of 14% BF3- Therefore, this study aims to (i) identify nutritional MeOH and incubating at 95°C for 1 hour.18 The biomarkers of fluid intelligence by empirically deriv- supernatant containing the fatty acid methyl esters ing patterns of n-3 PUFAs and (ii) distinguish the (FAMEs) was dried down under nitrogen, resuspended neural structures that mediate the beneficial effect of in 100 μl of hexane, transferred into amber GC vials, n-3 PUFAs on fluid intelligence. and stored at −20°C until the time of analysis. The phospholipid FAMEs were analyzed by a Materials and methods CLARUS 650 gas chromatograph (Perkin Elmer, Study participants Boston, MA, USA) equipped with a 100 m × This cross-sectional