Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-04T18:17:35.818Z Has data issue: false hasContentIssue false
  • English
  • Français

Fornix Microstructure and Memory Performance Is Associated with Altered Neural Connectivity during Episodic Recognition

Published online by Cambridge University Press:  18 February 2016

Martina Ly ,
Nagesh Adluru ,
Daniel J. Destiche ,
Sharon Y. Lu ,
Jennifer M. Oh ,
Siobhan M. Hoscheidt ,
Andrew L. Alexander ,
Ozioma C. Okonkwo ,
Howard A. Rowley  and
Mark A. Sager
...Show all authors
Martina Ly
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veteran’s Hospital, Madison, Wisconsin Alzheimer’s Disease Research Center, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin Wisconsin Alzheimer’s Institute, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin Neuroscience Training Program, University of Wisconsin, Madison, Wisconsin Waisman Laboratory for Brain Imaging and Behavior, University of Wisconsin, Madison, Wisconsin
Nagesh Adluru
Affiliation:
Waisman Laboratory for Brain Imaging and Behavior, University of Wisconsin, Madison, Wisconsin
Daniel J. Destiche
Affiliation:
Waisman Laboratory for Brain Imaging and Behavior, University of Wisconsin, Madison, Wisconsin
Sharon Y. Lu
Affiliation:
Waisman Laboratory for Brain Imaging and Behavior, University of Wisconsin, Madison, Wisconsin
Jennifer M. Oh
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veteran’s Hospital, Madison, Wisconsin Alzheimer’s Disease Research Center, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
Siobhan M. Hoscheidt
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veteran’s Hospital, Madison, Wisconsin Alzheimer’s Disease Research Center, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin Wisconsin Alzheimer’s Institute, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
Andrew L. Alexander
Affiliation:
Waisman Laboratory for Brain Imaging and Behavior, University of Wisconsin, Madison, Wisconsin Department of Psychiatry, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin Department of Medical Physics, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
Ozioma C. Okonkwo
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veteran’s Hospital, Madison, Wisconsin Alzheimer’s Disease Research Center, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin Wisconsin Alzheimer’s Institute, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
Howard A. Rowley
Affiliation:
Alzheimer’s Disease Research Center, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
Mark A. Sager
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veteran’s Hospital, Madison, Wisconsin Alzheimer’s Disease Research Center, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin Wisconsin Alzheimer’s Institute, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
Sterling C. Johnson
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veteran’s Hospital, Madison, Wisconsin Alzheimer’s Disease Research Center, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin Wisconsin Alzheimer’s Institute, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
Barbara B. Bendlin*
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veteran’s Hospital, Madison, Wisconsin Alzheimer’s Disease Research Center, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin Wisconsin Alzheimer’s Institute, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
*
Correspondence and reprint requests to: Barbara B. Bendlin, Department of Medicine and Alzheimer’s Disease Research Center, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin 53792. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives: The purpose of this study was to assess whether age-related differences in white matter microstructure are associated with altered task-related connectivity during episodic recognition. Methods: Using functional magnetic resonance imaging and diffusion tensor imaging from 282 cognitively healthy middle-to-late aged adults enrolled in the Wisconsin Registry for Alzheimer’s Prevention, we investigated whether fractional anisotropy (FA) within white matter regions known to decline with age was associated with task-related connectivity within the recognition network. Results: There was a positive relationship between fornix FA and memory performance, both of which negatively correlated with age. Psychophysiological interaction analyses revealed that higher fornix FA was associated with increased task-related connectivity amongst the hippocampus, caudate, precuneus, middle occipital gyrus, and middle frontal gyrus. In addition, better task performance was associated with increased task-related connectivity between the posterior cingulate gyrus, middle frontal gyrus, cuneus, and hippocampus. Conclusions: The findings indicate that age has a negative effect on white matter microstructure, which in turn has a negative impact on memory performance. However, fornix microstructure did not significantly mediate the effect of age on performance. Of interest, dynamic functional connectivity was associated with better memory performance. The results of the psychophysiological interaction analysis further revealed that alterations in fornix microstructure explain–at least in part–connectivity among cortical regions in the recognition memory network. Our results may further elucidate the relationship between structural connectivity, neural function, and cognition. (JINS, 2016, 22, 191–204)

Keywords

AgingTask-related functional connectivityfMRIgPPIFractional anisotropyEpisodic recognition
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 22 , Special Issue 2: Human Brain Connectivity in the Modern Era: Relevance to Understanding Health and Disease , February 2016 , pp. 191 - 204
Copyright
Copyright © The International Neuropsychological Society 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adluru, N., Destiche, D.J., Lu, S. Y.-F., Doran, S.T., Birdsill, A.C., Melah, K.E., & Bendlin, B.B. (2014). White matter microstructure in late middle-age: Effects of apolipoprotein E4 and parental family history of Alzheimer’s disease. Neuroimage. Clinical, 4, 730–742. http://doi.org/10.1016/j.nicl.2014.04.008 CrossRefGoogle ScholarPubMed
Aggleton, J.P., & Brown, M.W. (1999). Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. The Behavioral and Brain Sciences, 22(3), 425–444; discussion 444–489. http://doi.org/10.1017/S0140525X99002034 CrossRefGoogle ScholarPubMed
Aggleton, J.P., & Brown, M.W. (2006). Interleaving brain systems for episodic and recognition memory. Trends in Cognitive Sciences. http://doi.org/10.1016/j.tics.2006.08.003 CrossRefGoogle ScholarPubMed
Anderson, N.D., Iidaka, T., Cabeza, R., Kapur, S., McIntosh, A.R., & Craik, F.I. (2000). The effects of divided attention on encoding- and retrieval-related brain activity: A PET study of younger and older adults. Journal of Cognitive Neuroscience, 12(5), 775–792. http://doi.org/10.1162/089892900562598 CrossRefGoogle ScholarPubMed
Antonenko, D., Meinzer, M., Lindenberg, R., Witte, A.V., & Flöel, A. (2012). Grammar learning in older adults is linked to white matter microstructure and functional connectivity. Neuroimage, 62(3), 1667–1674. http://doi.org/10.1016/j.neuroimage.2012.05.074 CrossRefGoogle ScholarPubMed
Ashburner, J., & Friston, K.J. (1999). Nonlinear spatial normalization using basis functions. Human Brain Mapping, 7(4), 254–266. http://doi.org/10.1002/(SICI)1097-0193(1999)7:4<254::AID-HBM4>3.0.CO;2-G 3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Baddeley, A. (1996). Exploring the central executive. The Quarterly Journal of Experimental Psychology, 49A(1), 5–28.CrossRefGoogle Scholar
Beaulieu, C. (2002). The basis of anisotropic water diffusion in the nervous system - A technical review. NMR in Biomedicine, 15(7-8), 435–455. http://doi.org/10.1002/nbm.782 CrossRefGoogle ScholarPubMed
Benedict, R. (1997). Brief Visuospatial Memory Test-Revised. Odessa, FL: Psychological Assessment Resources, Inc.Google Scholar
Braak, H., & Braak, E. (1995). Staging of Alzheimer’s disease-related neurofibrillary changes. In Neurobiology of aging (Vol. 16, pp. 271–278). http://doi.org/10.1016/0197-4580(95)00021-6 Google Scholar
Cabeza, R. (2004). Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. Cerebral Cortex, 14(4), 364–375. http://doi.org/10.1093/cercor/bhg133 CrossRefGoogle ScholarPubMed
Cabeza, R., Anderson, N.D., Houle, S., Mangels, J.A., & Nyberg, L. (2000). Age-related differences in neural activity during item and temporal-order memory retrieval: A positron emission tomography study. Journal of Cognitive Neuroscience, 12(1), 197–206.CrossRefGoogle ScholarPubMed
Cabeza, R., & Dennis, N. (2012). Frontal lobes and aging: Deterioration and compensation. In Principles of frontal lobe function (pp. 628–652). http://doi.org/10.1093/acprof:oso/9780195134971.001.0001 Google Scholar
Cabeza, R., Grady, C.L., Nyberg, L., McIntosh, A.R., Tulving, E., Kapur, S., & Craik, F.I. (1997). Age-related differences in neural activity during memory encoding and retrieval: A positron emission tomography study. The Journal of Neuroscience, 17(1), 391–400. http://doi.org/0270-6474/96/170391-10$05.00/0 CrossRefGoogle ScholarPubMed
Cassel, J.C., Duconseille, E., Jeltsch, H., & Will, B. (1997). The fimbria-fornix/cingular bundle pathways: A review of neurochemical and behavioural approaches using lesions and transplantation techniques. Progress in Neurobiology, 51(6), 663–716. http://doi.org/10.1016/S0301-0082(97)00009-9 CrossRefGoogle ScholarPubMed
Catani, M., Howard, R.J., Pajevic, S., & Jones, D.K. (2002). Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage, 17(1), 77–94.CrossRefGoogle ScholarPubMed
Charlton, R.A., Schiavone, F., Barrick, T.R., Morris, R.G., & Markus, H.S. (2010). Diffusion tensor imaging detects age related white matter change over a 2 year follow-up which is associated with working memory decline. Journal of Neurology, Neurosurgery, and Psychiatry, 81(1), 13–19. http://doi.org/10.1136/jnnp.2008.167288 CrossRefGoogle Scholar
Crosby, E.C. (1962). Correlative anatomy of the nervous system. Macmillan. Retrieved from http://books.google.com/books/about/Correlative_anatomy_of_the_nervous_syste.html?id=zrRqAAAAMAAJ&pgis=1 Google Scholar
Daselaar, S.M., Fleck, M.S., Dobbins, I.G., Madden, D.J., & Cabeza, R. (2006). Effects of healthy aging on hippocampal and rhinal memory functions: An event-related fMRI study. Cerebral Cortex, 16(12), 1771–1782. http://doi.org/10.1093/cercor/bhj112 CrossRefGoogle ScholarPubMed
Davis, S.W., Dennis, N.A., Daselaar, S.M., Fleck, M.S., & Cabeza, R. (2008). Qué PASA? the posterior-anterior shift in aging. Cerebral Cortex, 18(5), 1201–1209. http://doi.org/10.1093/cercor/bhm155 CrossRefGoogle ScholarPubMed
Davis, S.W., Kragel, J.E., Madden, D.J., & Cabeza, R. (2012). The architecture of cross-hemispheric communication in the aging brain: Linking behavior to functional and structural connectivity. Cerebral Cortex, 22(1), 232–242. http://doi.org/10.1093/cercor/bhr123 CrossRefGoogle ScholarPubMed
Du, A.T., Schuff, N., Zhu, X.P., Jagust, W.J., Miller, B.L., Reed, B.R., & Weiner, M.W. (2003). Atrophy rates of entorhinal cortex in AD and normal aging. Neurology, 60(3), 481–486.CrossRefGoogle ScholarPubMed
Duverne, S., Motamedinia, S., & Rugg, M.D. (2009). The relationship between aging, performance, and the neural correlates of successful memory encoding. Cerebral Cortex, 19(3), 733–744. http://doi.org/10.1093/cercor/bhn122 CrossRefGoogle ScholarPubMed
Faure, A., Haberland, U., Condé, F., & El Massioui, N. (2005). Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation. The Journal of Neuroscience, 25(11), 2771–2780. http://doi.org/10.1523/JNEUROSCI.3894-04.2005 CrossRefGoogle Scholar
Finsterer, J., & Fuglsang-Frederiksen, A. (2000). Concentric needle EMG versus macro EMG I. Relation in healthy subjects. Clinical Neurophysiology, 111(7), 1211–1215. http://doi.org/10.1016/S1388-2457(00)00310-2 CrossRefGoogle ScholarPubMed
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). “Mini-mental state.” A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189–198. http://doi.org/10.1016/0022-3956(75)90026-6 CrossRefGoogle ScholarPubMed
Gläscher, J., Rudrauf, D., Colom, R., Paul, L.K., Tranel, D., Damasio, H., & Adolphs, R. (2010). Distributed neural system for general intelligence revealed by lesion mapping. Proceedings of the National Academy of Sciences of the United States of America, 107(10), 4705–4709. http://doi.org/10.1073/pnas.0910397107 CrossRefGoogle ScholarPubMed
Grady, C.L. (2008). Cognitive neuroscience of aging. Annals of the New York Academy of Sciences, 1124, 127–144. http://doi.org/10.1196/annals.1440.009 CrossRefGoogle ScholarPubMed
Grady, C.L., Grady, C.L., McIntosh, A.R., McIntosh, A.R., Craik, F.I.M., & Craik, F.I.M. (2005). Task-related activity in prefrontal cortex and its relation to recognition memory performance in young and old adults. Neuropsychologia, 43(10), 1466–1481. http://doi.org/10.1016/j.neuropsychologia.2004.12.016 CrossRefGoogle ScholarPubMed
Grady, C.L., McIntosh, A.R., & Craik, F.I.M. (2003). Age-related differences in the functional connectivity of the hippocampus during memory encoding. Hippocampus, 13(5), 572–586. http://doi.org/10.1002/hipo.10114 CrossRefGoogle ScholarPubMed
Greenwood, P.M. (2007). Functional plasticity in cognitive aging: Review and hypothesis. Neuropsychology, 21(6), 657–673. http://doi.org/10.1037/0894-4105.21.6.657 CrossRefGoogle ScholarPubMed
Gunning-Dixon, F.M., & Raz, N. (2000). The cognitive correlates of white matter abnormalities in normal aging: A quantitative review. Neuropsychology, 14(2), 224–232. http://doi.org/10.1037//0894-4105.14.2.224 CrossRefGoogle ScholarPubMed
Harvey, L.O. (1992). The critical operating characteristic and the evaluation of expert judgment. Organizational Behavior and Human Decision Processes. Available from http://doi.org/10.1016/0749-5978(92)90063-D CrossRefGoogle Scholar
Head, D., Kennedy, K.M., Rodrigue, K.M., & Raz, N. (2009). Age differences in perseveration: Cognitive and neuroanatomical mediators of performance on the Wisconsin Card Sorting Test. Neuropsychologia, 47(4), 1200–1203. http://doi.org/10.1016/j.neuropsychologia.2009.01.003 CrossRefGoogle ScholarPubMed
Hellyer, P.J., Shanahan, M., Scott, G., Wise, R.J.S., Sharp, D.J., & Leech, R. (2014). The control of global brain dynamics: Opposing actions of frontoparietal control and default mode networks on attention. The Journal of Neuroscience, 34(2), 451–461. http://doi.org/10.1523/JNEUROSCI.1853-13.2014 CrossRefGoogle ScholarPubMed
Jastak, S., & Wilkinson, G.S. (1984). The Wide Range Achievement test - Revised (Vol. III). Wilmington, DE: Jastak Associates.Google Scholar
Kaplan, E., Goodglass, H., & Weintraub, S. (1983). Boston Naming Test. Philadelphia: Lea & Febiger.Google Scholar
Kawas, C., Segal, J., Stewart, W.F., Corrada, M., & Thal, L.J. (1994). A validation study of the Dementia Questionnaire. Archives of Neurology, 51(9), 901–906. http://doi.org/10.1001/archneur.1994.00540210073015 CrossRefGoogle ScholarPubMed
Kehoe, E.G., Farrell, D., Metzler-Baddeley, C., Lawlor, B.A., Kenny, R.A., Lyons, D., & Bokde, A.L. (2015). Fornix white matter is correlated with resting-state functional connectivity of the thalamus and hippocampus in healthy aging but not in mild cognitive impairment - A preliminary study. Frontiers in Aging Neuroscience, 7, 10. http://doi.org/10.3389/fnagi.2015.00010 CrossRefGoogle Scholar
King, D.R., de Chastelaine, M., Elward, R.L., Wang, T.H., & Rugg, M.D. (2015). Recollection-related increases in functional connectivity predict individual differences in memory accuracy. Journal of Neuroscience, 35(4), 1763–1772. http://doi.org/10.1523/JNEUROSCI.3219-14.2015 CrossRefGoogle ScholarPubMed
Lamont, A.C., Stewart-Williams, S., & Podd, J. (2005). Face recognition and aging: Effects of target age and memory load. Memory & Cognition, 33(6), 1017–1024. http://doi.org/10.3758/BF03193209 CrossRefGoogle ScholarPubMed
Lockhart, S.N., Mayda, A.B.V., Roach, A.E., Fletcher, E., Carmichael, O., Maillard, P., & DeCarli, C. (2012). Episodic memory function is associated with multiple measures of white matter integrity in cognitive aging. Frontiers in Human Neuroscience, 6, 56. http://doi.org/10.3389/fnhum.2012.00056 CrossRefGoogle ScholarPubMed
Luk, G., Bialystok, E., Craik, F.I.M., & Grady, C.L. (2011). Lifelong bilingualism maintains white matter integrity in older adults. Journal of Neuroscience, 31(46), 16808–16813. http://doi.org/10.1523/JNEUROSCI.4563-11.2011 CrossRefGoogle ScholarPubMed
McKhann, G.M., Drachman, D., Folstein, M.F., Katzman, R., Price, D., & Stadlan, E.M. (1984). Clinical diagnosis of Alzheimer’s disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology, 34(7), 939–944. http://www.ncbi.nlm.nih.gov/pubmed/6610841 CrossRefGoogle ScholarPubMed
McKhann, G.M., Knopman, D.S., Chertkow, H., Hyman, B.T., Jack, C.R., Kawas, C.H., & Phelps, C.H. (2011). The diagnosis of dementia due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia, 7(3), 263–269. http://doi.org/10.1016/j.jalz.2011.03.005 CrossRefGoogle ScholarPubMed
McLaren, D.G., Ries, M.L., Xu, G., & Johnson, S.C. (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches. Neuroimage, 61(4), 1277–1286. http://doi.org/10.1016/j.neuroimage.2012.03.068 CrossRefGoogle ScholarPubMed
McLaren, D.G., Sperling, R.A., & Atri, A. (2014). Flexible modulation of network connectivity related to cognition in alzheimer’s disease. Neuroimage, 100, 544–557. http://doi.org/10.1016/j.neuroimage.2014.05.032 CrossRefGoogle ScholarPubMed
McNab, F., & Klingberg, T. (2008). Prefrontal cortex and basal ganglia control access to working memory. Nature Neuroscience, 11(1), 103–107. http://doi.org/10.1038/nn2024 CrossRefGoogle ScholarPubMed
Metzler-Baddeley, C., Jones, D.K., Belaroussi, B., Aggleton, J.P., & O’Sullivan, M.J. (2011). Frontotemporal connections in episodic memory and aging: A diffusion MRI tractography study. The Journal of Neuroscience, 31(37), 13236–13245. http://doi.org/10.1523/JNEUROSCI.2317-11.2011 CrossRefGoogle ScholarPubMed
Morcom, A.M., Good, C.D., Frackowiak, R.S.J., & Rugg, M.D. (2003). Age effects on the neural correlates of successful memory encoding. Brain, 126(1), 213–229. http://doi.org/10.1093/brain/awg020 CrossRefGoogle ScholarPubMed
Nandedkar, S., & Stalberg, E. (1983). Simulation of macro EMG motor unit potentials. Electroencephalography and Clinical Neurophysiology, 56(1), 52–62. http://doi.org/10.1016/0013-4694(83)90006-8 CrossRefGoogle ScholarPubMed
Nicholas, C.R., Okonkwo, O.C., Bendlin, B.B., Oh, J.M., Asthana, S., Rowley, H.A., & Johnson, S.C. (2014). Posteromedial hyperactivation during episodic recognition among people with memory decline: Findings from the WRAP study. Brain Imaging and Behavior. [Epub ahead of print]. http://doi.org/10.1007/s11682-014-9322-z Google Scholar
O’Sullivan, M., Jones, D.K., Summers, P.E., Morris, R.G., Williams, S.C., & Markus, H.S. (2001). Evidence for cortical “disconnection” as a mechanism of age-related cognitive decline. Neurology, 57(4), 632–638. http://doi.org/10.1212/WNL.57.4.632 CrossRefGoogle ScholarPubMed
Persson, J., Nyberg, L., Lind, J., Larsson, A., Nilsson, L.G., Ingvar, M., & Buckner, R.L. (2006). Structure-function correlates of cognitive decline in aging. Cerebral Cortex, 16(7), 907–915. http://doi.org/10.1093/cercor/bhj036 CrossRefGoogle ScholarPubMed
Pfefferbaum, A., Adalsteinsson, E., & Sullivan, E.V. (2005). Frontal circuitry degradation marks healthy adult aging: Evidence from diffusion tensor imaging. Neuroimage, 26(3), 891–899. http://doi.org/10.1016/j.neuroimage.2005.02.034 CrossRefGoogle ScholarPubMed
Poletti, C.E., & Creswell, G. (1977). Fornix system efferent projections in the squirrel monkey: An experimental degeneration study. The Journal of Comparative Neurology, 175(1), 101–128. http://doi.org/10.1002/cne.901750107 CrossRefGoogle ScholarPubMed
Rajah, M.N., Languay, R., & Grady, C.L. (2011). Age-related changes in right middle frontal gyrus volume correlate with altered episodic retrieval activity. Journal of Neuroscience, 31(49), 17941–17954. http://doi.org/10.1523/JNEUROSCI.1690-11.2011 CrossRefGoogle ScholarPubMed
Raz, N., Rodrigue, K.M., Kennedy, K.M., Dahle, C., Head, D., & Acker, J.D. (2003). Differential age-related changes in the regional metencephalic volumes in humans: A 5-year follow-up. Neuroscience Letters, 349(3), 163–166. http://doi.org/10.1016/S0304-3940(03)00820-6 CrossRefGoogle ScholarPubMed
Reitan, R., & Wolfson, D. (1993). The Halstead-Reitan Neuropsychological Test Battery: Theory and clinical interpretation. Tucson, AZ: Neuropsychology Press.Google Scholar
Rodrigue, K.M., & Raz, N. (2004). Shrinkage of the entorhinal cortex over five years predicts memory performance in healthy adults. The Journal of Neuroscience, 24(4), 956–963. http://doi.org/10.1523/JNEUROSCI.4166-03.2004 CrossRefGoogle ScholarPubMed
Rudebeck, S.R., Scholz, J., Millington, R., Rohenkohl, G., Johansen-Berg, H., & Lee, A.C.H. (2009). Fornix microstructure correlates with recollection but not familiarity memory. The Journal of Neuroscience, 29(47), 14987–14992. http://doi.org/10.1523/JNEUROSCI.4707-09.2009 CrossRefGoogle Scholar
Rugg, M.D., & Vilberg, K.L. (2013). Brain networks underlying episodic memory retrieval. Current Opinion in Neurobiology, 23(2), 255–260. http://doi.org/10.1016/j.conb.2012.11.005 CrossRefGoogle ScholarPubMed
Sadeh, T., Shohamy, D., Levy, D.R., Reggev, N., & Maril, A. (2011). Cooperation between the hippocampus and the striatum during episodic encoding. Journal of Cognitive Neuroscience, 23(7), 1597–1608. http://doi.org/10.1162/jocn.2010.21549 CrossRefGoogle ScholarPubMed
Sager, M.A., Hermann, B., & La Rue, A. (2005). Middle-aged children of persons with Alzheimer’s disease: APOE genotypes and cognitive function in the Wisconsin Registry for Alzheimer’s Prevention. Journal of Geriatric Psychiatry and Neurology, 18(4), 245–249. http://doi.org/10.1177/0891988705281882 CrossRefGoogle ScholarPubMed
Salami, A., Pudas, S., & Nyberg, L. (2014). Elevated hippocampal resting-state connectivity underlies deficient neurocognitive function in aging. Proceedings of the National Academy of Sciences of the United States of America, 111(49), 17654–17659. http://doi.org/10.1073/pnas.1410233111 CrossRefGoogle ScholarPubMed
Schacter, D.L., Savage, C.R., Alpert, N.M., Rauch, S.L., & Albert, M.S. (1996). The role of hippocampus and frontal cortex in age-related memory changes: A PET study. Neuroreport, 7(6), 1165–1169.CrossRefGoogle ScholarPubMed
Schedlbauer, A.M., Copara, M.S., Watrous, A.J., & Ekstrom, A.D. (2014). Multiple interacting brain areas underlie successful spatiotemporal memory retrieval in humans. Scientific Reports, 4, 6431. http://doi.org/10.1038/srep06431 CrossRefGoogle ScholarPubMed
Schiavetto, A., Köhler, S., Grady, C.L., Winocur, G., & Moscovitch, M. (2002). Neural correlates of memory for object identity and object location: Effects of aging. Neuropsychologia, 40(8), 1428–1442. http://doi.org/10.1016/S0028-3932(01)00206-8 CrossRefGoogle ScholarPubMed
Schmahmann, J.D., & Pandya, D.N. (2007). The complex history of the fronto-occipital fasciculus. Journal of the History of the Neurosciences, 16(4), 362–377. http://doi.org/10.1080/09647040600620468 CrossRefGoogle ScholarPubMed
Schmidt, M. (1996). Rey Auditory Verbal Learning Test: RAVLT : A Handbook. Western Psychological Services. Retrieved from http://books.google.com/books/about/Rey_Auditory_Verbal_Learning_Test.html?id=UOcPRAAACAAJ&pgis=1 Google Scholar
Staresina, B.P., Cooper, E., & Henson, R.N. (2013). Reversible information flow across the medial temporal lobe: The hippocampus links cortical modules during memory retrieval. The Journal of Neuroscience, 33(35), 14184–14192. http://doi.org/10.1523/JNEUROSCI.1987-13.2013 CrossRefGoogle ScholarPubMed
Steffener, J., Habeck, C.G., & Stern, Y. (2012). Age-related changes in task related functional network connectivity. PLoS One, 7(9), e44421. http://doi.org/10.1371/journal.pone.0044421 CrossRefGoogle ScholarPubMed
Takahashi, S., Yonezawa, H., Takahashi, J., Kudo, M., Inoue, T., & Tohgi, H. (2002). Selective reduction of diffusion anisotropy in white matter of Alzheimer disease brains measured by 3.0 Tesla magnetic resonance imaging. Neuroscience Letters, 332(1), 45–48. http://doi.org/S030439400200914X [pii].CrossRefGoogle ScholarPubMed
Tang, Y., Nyengaard, J.R., Pakkenberg, B., & Gundersen, H.J. (1997). Age-induced white matter changes in the human brain: a stereological investigation. Neurobiology of Aging, 18(6), 600–615.CrossRefGoogle Scholar
Trenerry, M., Crosson, B., Deboe, J., & Leber, L. (1989). Stroop Neuropsychological Screening Test. Odessa, FL: Psychological Assessment Resources, Inc.Google Scholar
Tulving, E. (1984). Precis of elements of episodic. The Behavioral and Brain Sciences, 7(2), 223–268. http://doi.org/http://dx.doi.org/10.1017/S0140525X0004440X CrossRefGoogle Scholar
Vakil, E., Blachstein, H., & Soroker, N. (2004). Differential effect of right and left basal ganglionic infarctions on procedural learning. Cognitive and Behavioral Neurology, 17(2), 62–73. http://doi.org/10.1097/01.wnn.0000094553.44085.25 CrossRefGoogle ScholarPubMed
Wakana, S., Jiang, H., Nagae-Poetscher, L.M., van Zijl, P.C.M., & Mori, S. (2004). Fiber tract-based atlas of human white matter anatomy. Radiology, 230(1), 77–87. http://doi.org/10.1148/radiol.2301021640 CrossRefGoogle ScholarPubMed
Wang, Y., Gupta, A., Liu, Z., Zhang, H., Escolar, M.L., Gilmore, J.H., & Styner, M. (2011). DTI registration in atlas based fiber analysis of infantile Krabbe disease. Neuroimage, 55(4), 1577–1586. http://doi.org/10.1016/j.neuroimage.2011.01.038 CrossRefGoogle ScholarPubMed
Watrous, A.J., Tandon, N., Conner, C.R., Pieters, T., & Ekstrom, A.D. (2013). Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. Nature Neuroscience, 16(3), 349–356. http://doi.org/10.1038/nn.3315 CrossRefGoogle ScholarPubMed
Williams, Z.M., & Eskandar, E.N. (2006). Selective enhancement of associative learning by microstimulation of the anterior caudate. Nature Neuroscience, 9(4), 562–568. http://doi.org/10.1038/nn1662 CrossRefGoogle ScholarPubMed
Xu, G., McLaren, D.G., Ries, M.L., Fitzgerald, M.E., Bendlin, B.B., Rowley, H.A., & Johnson, S.C. (2009). The influence of parental history of Alzheimer’s disease and apolipoprotein E epsilon4 on the BOLD signal during recognition memory. Brain, 132(Pt 2), 383–391. http://doi.org/10.1093/brain/awn254 CrossRefGoogle ScholarPubMed
Yin, H.H., Ostlund, S.B., Knowlton, B.J., & Balleine, B.W. (2005). The role of the dorsomedial striatum in instrumental conditioning. European Journal of Neuroscience, 22(2), 513–523. http://doi.org/10.1111/j.1460-9568.2005.04218.x CrossRefGoogle ScholarPubMed
Yonelinas, A.P., Widaman, K., Mungas, D., Reed, B., Weiner, M.W., & Chui, H.C. (2007). Memory in the aging brain: Doubly dissociating the contribution of the hippocampus and entorhinal cortex. Hippocampus, 17(11), 1134–1140. http://doi.org/10.1002/hipo.20341 CrossRefGoogle ScholarPubMed
Zahr, N.M., Rohlfing, T., Pfefferbaum, A., & Sullivan, E.V. (2009). Problem solving, working memory, and motor correlates of association and commissural fiber bundles in normal aging: A quantitative fiber tracking study. Neuroimage, 44(3), 1050–1062. http://doi.org/10.1016/j.neuroimage.2008.09.046 CrossRefGoogle ScholarPubMed
Zhang, H., Avants, B.B., Yushkevich, P.A., Woo, J.H., Wang, S., McCluskey, L.F., & Gee, J.C. (2007). High-dimensional spatial normalization of diffusion tensor images improves the detection of white matter differences: An example study using amyotrophic lateral sclerosis. IEEE Transactions on Medical Imaging, 26(11), 1585–1597. http://doi.org/10.1109/TMI.2007.906784 CrossRefGoogle ScholarPubMed
Zhang, H., Yushkevich, P.A., Alexander, D.C., & Gee, J.C. (2006). Deformable registration of diffusion tensor MR images with explicit orientation optimization. Medical Image Analysis, 10(5), 764–785. http://doi.org/10.1016/j.media.2006.06.004 CrossRefGoogle ScholarPubMed
Zhang, H., Yushkevich, P.A., Rueckert, D., & Gee, J.C. (2007). Unbiased white matter atlas construction using diffusion tensor images. Medical Image Computing and Computer-Assisted Intervention, 10(Pt 2), 211–218.Google ScholarPubMed
Zhuang, L., Sachdev, P.S., Trollor, J.N., Kochan, N.A., Reppermund, S., Brodaty, H., & Wen, W. (2012). Microstructural white matter changes in cognitively normal individuals at risk of amnestic MCI. Neurology, 79(8), 748–754. http://doi.org/10.1212/WNL.0b013e3182661f4d CrossRefGoogle ScholarPubMed