{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,12]],"date-time":"2026-05-12T02:30:40Z","timestamp":1778553040942,"version":"3.51.4"},"reference-count":63,"publisher":"MIT Press - Journals","issue":"2","content-domain":{"domain":["direct.mit.edu"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2012,2,1]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Few studies have investigated how aging influences the neural basis of implicit associative learning, and available evidence is inconclusive. One emerging behavioral pattern is that age differences increase with practice, perhaps reflecting the involvement of different brain regions with training. Many studies report hippocampal involvement early on with learning becoming increasingly dependent on the caudate with practice. We tested the hypothesis that the contribution of these regions to learning changes with age because of differential age-related declines in the striatum and hippocampi. We assessed age-related differences in brain activation during implicit associative learning using the Triplets Learning Task. Over three event-related fMRI runs, 11 younger and 12 healthy older adults responded to only the third (target) stimulus in sequences of three stimuli (\u201ctriplets\u201d) by corresponding key press. Unbeknown to participants, the first stimulus' location predicted one target location for 80% of trials and another target location for 20% of trials. Both age groups learned associative regularities but differences in favor of the younger adults emerged with practice. The neural basis of learning (response to predictability) was examined by identifying regions that showed a greater response to triplets that occurred more frequently. Both age groups recruited the hippocampus early, but with training, the younger adults recruited their caudate whereas the older adults continued to rely on their hippocampus. This pattern enables older adults to maintain near-young levels of performance early in training, but not later, and adds to evidence that implicit associative learning is supported by different brain networks in younger and older adults.<\/jats:p>","DOI":"10.1162\/jocn_a_00116","type":"journal-article","created":{"date-parts":[[2011,8,23]],"date-time":"2011-08-23T20:18:41Z","timestamp":1314130721000},"page":"451-463","update-policy":"https:\/\/doi.org\/10.1162\/mitpressjournals.corrections.policy","source":"Crossref","is-referenced-by-count":43,"title":["The Effects of Aging on the Neural Basis of Implicit Associative Learning in a Probabilistic Triplets Learning Task"],"prefix":"10.1162","volume":"24","author":[{"given":"Jessica R.","family":"Simon","sequence":"first","affiliation":[{"name":"1Georgetown University"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chandan J.","family":"Vaidya","sequence":"additional","affiliation":[{"name":"1Georgetown University"},{"name":"2Children's National Medical Center, Washington, DC"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"suffix":"Jr.","given":"James H.","family":"Howard","sequence":"additional","affiliation":[{"name":"1Georgetown University"},{"name":"3Catholic University of America, Washington, DC"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Darlene V.","family":"Howard","sequence":"additional","affiliation":[{"name":"1Georgetown University"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"281","published-online":{"date-parts":[[2012,2,1]]},"reference":[{"key":"2021072913173443300_R1","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1016\/j.neurobiolaging.2005.03.017","article-title":"Prefrontal and striatal activation in elderly subjects during concurrent implicit and explicit sequence learning.","volume":"27","author":"Aizenstein","year":"2006","journal-title":"Neurobiology of Aging"},{"key":"2021072913173443300_R2","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1016\/j.tics.2010.02.001","article-title":"Cortical and basal ganglia contributions to habit learning and automaticity.","volume":"14","author":"Ashby","year":"2010","journal-title":"Trends in Cognitive Sciences"},{"key":"2021072913173443300_R3","doi-asserted-by":"crossref","first-page":"P98","DOI":"10.1093\/geronb\/62.2.P98","article-title":"Age-related differences in implicit learning of subtle third-order sequential structure.","volume":"62","author":"Bennett","year":"2007","journal-title":"Journals of Gerontology, Series B: Psychological Sciences and Social Sciences"},{"key":"2021072913173443300_R4","article-title":"White matter integrity correlates of implicit sequence learning in healthy aging.","author":"Bennett","year":"","journal-title":"Neurobiology of Aging"},{"key":"2021072913173443300_R5","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1196\/annals.1416.006","article-title":"Two forms of implicit learning in young adults with dyslexia.","volume":"1145","author":"Bennett","year":"2008","journal-title":"Annals of the New York Academy of Sciences"},{"key":"2021072913173443300_R6","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1007\/s00426-004-0207-4","article-title":"Processing abstract sequence structure: Learning without knowing, or knowing without learning?","volume":"69","author":"Boyer","year":"2005","journal-title":"Psychological Research"},{"key":"2021072913173443300_R7","unstructured":"Brett, M., Anton, J.-L., Valabregue, R., & Poline, J.-B. (2002). Region of interest analysis using an SPM toolbox, Paper presented at the 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan."},{"key":"2021072913173443300_R8","doi-asserted-by":"crossref","first-page":"844","DOI":"10.1038\/12222","article-title":"Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage.","volume":"2","author":"Chun","year":"1999","journal-title":"Nature Neuroscience"},{"key":"2021072913173443300_R9","unstructured":"Ciomek, N., Song, S. S., Howard, J. H., & Howard, D. V. (2007). Age deficits in probabilistic category learning, Paper presented at the Association for Psychological Science, Washington, DC."},{"key":"2021072913173443300_R10","first-page":"491","article-title":"Models of implicit learning. In","volume-title":"Encyclopedia of cognitive science","author":"Cleeremans","year":"2002"},{"key":"2021072913173443300_R11","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1002\/(SICI)1097-0193(1999)8:2\/3<109::AID-HBM7>3.0.CO;2-W","article-title":"Optimal experimental design for event-related fMRI.","volume":"8","author":"Dale","year":"1999","journal-title":"Human Brain Mapping"},{"key":"2021072913173443300_R12","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1016\/S0197-4580(03)00030-7","article-title":"Similar network activated by young and old adults during the acquisition of a motor sequence.","volume":"24","author":"Daselaar","year":"2003","journal-title":"Neurobiology of Aging"},{"key":"2021072913173443300_R13","doi-asserted-by":"crossref","first-page":"1201","DOI":"10.1093\/cercor\/bhm155","article-title":"Que PASA? The posterior-anterior shift in aging.","volume":"18","author":"Davis","year":"2008","journal-title":"Cerebral Cortex"},{"key":"2021072913173443300_R14","first-page":"1","article-title":"Neuroimaging in cognitive aging.","volume-title":"Handbook of aging and cognition","author":"Dennis","year":"2008","edition":"3rd ed."},{"key":"2021072913173443300_R15","article-title":"Age-related dedifferentiation of learning systems: An fMRI study of implicit and explicit learning.","author":"Dennis","year":"","journal-title":"Neurobiology of Aging"},{"key":"2021072913173443300_R16","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1007\/s00221-006-0534-3","article-title":"Implicit sequence learning without motor sequencing in young and old adults.","volume":"175","author":"Dennis","year":"2006","journal-title":"Experimental Brain Research"},{"key":"2021072913173443300_R17","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1097\/WCO.0b013e328304b6a3","article-title":"Motor sequence learning and movement disorders.","volume":"21","author":"Doyon","year":"2008","journal-title":"Current Opinion in Neurology"},{"key":"2021072913173443300_R18","doi-asserted-by":"crossref","first-page":"11340","DOI":"10.1523\/JNEUROSCI.2736-05.2005","article-title":"Neural mechanisms underlying probabilistic category learning in normal aging.","volume":"25","author":"Fera","year":"2005","journal-title":"Journal of Neuroscience"},{"key":"2021072913173443300_R19","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1037\/0882-7974.19.1.171","article-title":"A quantitative model-based approach to examining aging effects on information-integration category learning.","volume":"19","author":"Filoteo","year":"2004","journal-title":"Psychology and Aging"},{"key":"2021072913173443300_R20","first-page":"47","article-title":"One concept, multiple meanings: On how to deine the concept of implicit learning.","volume-title":"Handbook of implicit learning","author":"Frensch","year":"1998"},{"key":"2021072913173443300_R21","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1080\/09541440802257423","article-title":"Effects of age and practice in sequence learning: A graded account of aging, learning and control.","volume":"21","author":"Gaillard","year":"2009","journal-title":"European Journal of Cognitive Psychology"},{"key":"2021072913173443300_R22","volume-title":"Gateway to memory: An introduction to neural network models of the hippocampus and learning.","author":"Gluck","year":"2001"},{"key":"2021072913173443300_R23","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1162\/jocn.1995.7.4.497","article-title":"Functional mapping of sequence learning in normal humans.","volume":"7","author":"Grafton","year":"1995","journal-title":"Journal of Cognitive Neuroscience"},{"key":"2021072913173443300_R24","first-page":"1501","article-title":"Differential aging of the human striatum: A prospective MR imaging study.","volume":"19","author":"Gunning-Dixon","year":"1998","journal-title":"American Journal of Neuroradiology"},{"key":"2021072913173443300_R25","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.tins.2005.02.004","article-title":"Complementary memory systems: Competition, cooperation and compensation.","volume":"28","author":"Hartley","year":"2005","journal-title":"Trends in Neurosciences"},{"key":"2021072913173443300_R26","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1093\/cercor\/bhh174","article-title":"Frontal-hippocampal double dissociation between normal aging and Alzheimer's disease.","volume":"15","author":"Head","year":"2005","journal-title":"Cerebral Cortex"},{"key":"2021072913173443300_R27","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1038\/nrn1323","article-title":"Insights into the ageing mind: A view from cognitive neuroscience.","volume":"5","author":"Hedden","year":"2004","journal-title":"Nature Reviews Neuroscience"},{"key":"2021072913173443300_R28","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1038\/nrn2850","article-title":"A model for memory systems based on processing modes rather than consciousness.","volume":"11","author":"Henke","year":"2010","journal-title":"Nature Reviews Neuroscience"},{"key":"2021072913173443300_R29","article-title":"Dissociable forms of implicit learning in aging.","volume-title":"Perspectives on human memory and aging.","author":"Howard","year":""},{"key":"2021072913173443300_R30","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1037\/0882-7974.19.1.79","article-title":"Implicit sequence learning: Effects of level of structure, adult age, and extended practice.","volume":"19","author":"Howard","year":"2004","journal-title":"Psychology and Aging"},{"key":"2021072913173443300_R31","doi-asserted-by":"crossref","first-page":"634","DOI":"10.1037\/0882-7974.12.4.634","article-title":"Age differences in implicit learning of higher order dependencies in serial patterns.","volume":"12","author":"Howard","year":"1997","journal-title":"Psychology and Aging"},{"key":"2021072913173443300_R32","first-page":"1139","article-title":"Implicit learning of predictive relationships in three-element visual sequences by young and old adults.","volume":"34","author":"Howard","year":"2008","journal-title":"Journal of Experimental Psychology: Learning, Memory, and Cognition"},{"key":"2021072913173443300_R33","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1080\/13825580601186635","article-title":"Event timing and age deficits in higher-order sequence learning.","volume":"14","author":"Howard","year":"2007","journal-title":"Neuropsychology, Development, and Cognition, Section B: Aging, Neuropsychology, and Cognition"},{"key":"2021072913173443300_R34","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1080\/13825580601139444","article-title":"Associative learning over trials activates the hippocampus in healthy elderly but not mild cognitive impairment.","volume":"15","author":"Johnson","year":"2008","journal-title":"Aging, Neuropsychology, and Cognition"},{"key":"2021072913173443300_R35","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1016\/S0959-4388(97)80033-5","article-title":"Learning perceptual skills: Behavioral probes into adult cortical plasticity.","volume":"7","author":"Karni","year":"1997","journal-title":"Current Opinion in Neurobiology"},{"key":"2021072913173443300_R36","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1101\/lm.1.2.106","article-title":"Probabilistic classification learning in amnesia.","volume":"1","author":"Knowlton","year":"1994","journal-title":"Learning and Memory"},{"key":"2021072913173443300_R37","doi-asserted-by":"crossref","first-page":"2998","DOI":"10.1016\/j.neuropsychologia.2010.06.008","article-title":"Rule-based and information-integration category learning in normal aging.","volume":"48","author":"Maddox","year":"2010","journal-title":"Neuropsychologia"},{"key":"2021072913173443300_R38","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1101\/lm.43006","article-title":"Strategies in probabilistic categorization: Results from a new way of analyzing performance.","volume":"13","author":"Meeter","year":"2006","journal-title":"Learning and Memory"},{"key":"2021072913173443300_R39","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1037\/0735-7044.118.2.438","article-title":"An implicit learning task activates medial temporal lobe in patients with Parkinson's disease.","volume":"118","author":"Moody","year":"2004","journal-title":"Behavioral Neuroscience"},{"key":"2021072913173443300_R40","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0010-0285(87)90002-8","article-title":"Attentional requirements of learning: Evidence from performance measures.","volume":"19","author":"Nissen","year":"1987","journal-title":"Cognitive Psychology"},{"key":"2021072913173443300_R41","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1037\/0882-7974.23.1.104","article-title":"Differential effects of age on item and associative measures of memory: A meta-analysis.","volume":"23","author":"Old","year":"2008","journal-title":"Psychology and Aging"},{"key":"2021072913173443300_R42","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1038\/35107080","article-title":"Interactive memory systems in the human brain.","volume":"414","author":"Poldrack","year":"2001","journal-title":"Nature"},{"key":"2021072913173443300_R43","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/S0028-3932(02)00157-4","article-title":"Competition among multiple memory systems: Converging evidence from animal and human brain studies.","volume":"41","author":"Poldrack","year":"2003","journal-title":"Neuropsychologia"},{"key":"2021072913173443300_R44","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.neurobiolaging.2004.12.013","article-title":"Hippocampal and neocortical activation during repetitive encoding in older persons.","volume":"27","author":"Rand-Giovannetti","year":"2006","journal-title":"Neurobiology of Aging"},{"key":"2021072913173443300_R45","doi-asserted-by":"crossref","first-page":"1676","DOI":"10.1093\/cercor\/bhi044","article-title":"Regional brain changes in aging healthy adults: General trends, individual differences and modifiers.","volume":"15","author":"Raz","year":"2005","journal-title":"Cerebral Cortex"},{"key":"2021072913173443300_R46","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1212\/01.WNL.0000106466.09835.46","article-title":"Differential aging of the medial temporal lobe: A study of a five-year change.","volume":"62","author":"Raz","year":"2004","journal-title":"Neurology"},{"key":"2021072913173443300_R47","first-page":"1849","article-title":"Differential aging of the human striatum: Longitudinal evidence.","volume":"24","author":"Raz","year":"2003","journal-title":"AJNR, American Journal of Neuroradiology"},{"key":"2021072913173443300_R48","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1002\/1097-0029(20001001)51:1<85::AID-JEMT9>3.0.CO;2-0","article-title":"Neuroanatomical and cognitive correlates of adult age differences in acquisition of a perceptual-motor skill.","volume":"51","author":"Raz","year":"2000","journal-title":"Microscopy Research & Technique"},{"key":"2021072913173443300_R49","first-page":"88","article-title":"Implicit learning of synthetic languages: The role of instructional set.","volume":"2","author":"Reber","year":"1976","journal-title":"Journal of Experimental Psychology: Human Learning & Memory"},{"key":"2021072913173443300_R50","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1111\/j.1467-8721.2008.00570.x","article-title":"Neurocognitive aging and the compensation hypothesis.","volume":"17","author":"Reuter-Lorenz","year":"2008","journal-title":"Current Directions in Psychological Science"},{"key":"2021072913173443300_R51","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1007\/s11065-009-9117-y","article-title":"Implicit learning in aging: Extant patterns and new directions.","volume":"19","author":"Rieckmann","year":"2009","journal-title":"Neuropsychology Review"},{"key":"2021072913173443300_R52","doi-asserted-by":"crossref","first-page":"1303","DOI":"10.1016\/j.neuroimage.2010.01.015","article-title":"Activation in striatum and medial temporal lobe during sequence learning in younger and older adults: Relations to performance.","volume":"50","author":"Rieckmann","year":"2010","journal-title":"Neuroimage"},{"key":"2021072913173443300_R53","doi-asserted-by":"crossref","first-page":"1221","DOI":"10.1016\/S0896-6273(02)01105-4","article-title":"The role of medial temporal lobe structures in implicit learning: An event-related fMRI study.","volume":"36","author":"Rose","year":"2002","journal-title":"Neuron"},{"key":"2021072913173443300_R54","doi-asserted-by":"crossref","first-page":"1597","DOI":"10.1162\/jocn.2010.21549","article-title":"Cooperation between the hippocampus and the striatum during episodic encoding.","volume":"23","author":"Sadeh","year":"2011","journal-title":"Journal of Cognitive Neuroscience"},{"key":"2021072913173443300_R55","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1076\/anec.6.1.1.789","article-title":"A framework for analyzing and interpreting differential aging patterns: Application to three measures of implicit learning.","volume":"6","author":"Salthouse","year":"1999","journal-title":"Aging, Neuropsychology and Cognition"},{"key":"2021072913173443300_R56","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1016\/S0896-6273(03)00123-5","article-title":"An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning.","volume":"37","author":"Schendan","year":"2003","journal-title":"Neuron"},{"key":"2021072913173443300_R57","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/j.neubiorev.2007.07.008","article-title":"Basal ganglia and dopamine contributions to probabilistic category learning.","volume":"32","author":"Shohamy","year":"2008","journal-title":"Neuroscience and Biobehavioral Reviews"},{"key":"2021072913173443300_R58","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1093\/geronb\/gbq066","article-title":"Age differences in implicit learning of probabilistic, unstructured sequences.","volume":"66","author":"Simon","year":"2011","journal-title":"Journals of Gerontology, Series B: Psychological Sciences and Social Sciences"},{"key":"2021072913173443300_R59","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1016\/j.bbr.2010.08.043","article-title":"Dopamine transporter genotype predicts implicit sequence learning.","volume":"216","author":"Simon","year":"2011","journal-title":"Behavioural Brain Research"},{"key":"2021072913173443300_R60","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1016\/j.neurobiolaging.2004.09.015","article-title":"Preservation of hippocampal volume throughout adulthood in healthy men and women.","volume":"26","author":"Sullivan","year":"2005","journal-title":"Neurobiology of Aging"},{"key":"2021072913173443300_R61","doi-asserted-by":"crossref","first-page":"1934","DOI":"10.1162\/jocn.2009.21131","article-title":"Neural evidence of statistical learning: Efficient detection of visual regularities without awareness.","volume":"21","author":"Turk-Browne","year":"2009","journal-title":"Journal of Cognitive Neuroscience"},{"key":"2021072913173443300_R62","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1006\/nimg.2001.0978","article-title":"Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.","volume":"15","author":"Tzourio-Mazoyer","year":"2002","journal-title":"Neuroimage"},{"key":"2021072913173443300_R63","unstructured":"Ward, B. D. (2000). Simultaneous inference for fMRI data. Available at http:\/\/afni.nimh.nih.gov\/pub\/dist\/doc\/manual\/AlphaSim.pdf."}],"container-title":["Journal of Cognitive Neuroscience"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/direct.mit.edu\/jocn\/article-pdf\/24\/2\/451\/1943232\/jocn_a_00116.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/direct.mit.edu\/jocn\/article-pdf\/24\/2\/451\/1943232\/jocn_a_00116.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,12,1]],"date-time":"2021-12-01T14:35:26Z","timestamp":1638369326000},"score":1,"resource":{"primary":{"URL":"https:\/\/direct.mit.edu\/jocn\/article\/24\/2\/451\/27728\/The-Effects-of-Aging-on-the-Neural-Basis-of"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2012,2,1]]},"references-count":63,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2012,2,1]]},"published-print":{"date-parts":[[2012,2,1]]}},"URL":"https:\/\/doi.org\/10.1162\/jocn_a_00116","relation":{},"ISSN":["0898-929X","1530-8898"],"issn-type":[{"value":"0898-929X","type":"print"},{"value":"1530-8898","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2012,2]]},"published":{"date-parts":[[2012,2,1]]}}}