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Implicit Learning in Aging: Extant Patterns and New Directions

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Abstract

Research suggests that the striatum plays an important role in implicit learning (IL). The striatum exhibits marked age-related morphological and neurochemical losses. Yet, behavioral studies suggest that IL is generally well preserved in old age, and that age-related differences emerge only when highly complex IL tasks are used. In this review, we integrate behavioral and neuroimaging evidence on IL in aging. We suggest that relative stability of IL in old age may reflect neural reorganization that compensates for age-related losses in striatal functions. Specifically, there may be an age-related increase in reliance on extrastriatal regions (e.g., medial-temporal, frontal) during IL. This reorganization of function may be beneficial under less taxing performance conditions, but not when task demands become more challenging.

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References

  • Aizenstein, H. J., Butters, M. A., Clark, K. A., Figurski, J. L., Stenger, V. A., Nebes, R. D., et al. (2005). Prefrontal and striatal activation in elderly subjects during concurrent implicit and explicit sequence learning. Neurobiology of Aging, 27, 741–751.

    Article  PubMed  Google Scholar 

  • Albouy, G., Sterpenich, V., Balteau, E., Vandewalle, G., Desseilles, M., Dang-Vu, T., et al. (2008). Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron, 58, 261–272.

    Article  CAS  PubMed  Google Scholar 

  • Alexander, G. E., Crutcher, M. D., & DeLong, M. R. (1990). Basal ganglia-thalamocortical circuits: Parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. Progress in Brain Research, 85, 119–146.

    Article  CAS  PubMed  Google Scholar 

  • Allen, J. S., Bruss, J., Brown, C. K., & Damasio, H. (2005). Neurobiology of Aging, 26, 1245–1260.

    Article  PubMed  Google Scholar 

  • Atallah, H. E., Lopez-Paniagua, D., Rudy, J. W., & O’Reilly, R. C. (2007). Separate neural substrates for skill learning and performance in the ventral and dorsal striatum. Nature Neuroscience, 10, 126–131.

    Article  CAS  PubMed  Google Scholar 

  • Bäckman, L., Almkvist, O., Andersson, J., Nordberg, A., Winblad, B., Reineck, R., et al. (1997). Brain activation in young and older adults during implicit and explicit retrieval. Journal of Cognitive Neuroscience, 9, 378–391.

    Article  Google Scholar 

  • Bäckman, L., Almkvist, O., Nyberg, L., & Andersson, J. (2000). Functional changes in brain activity during priming in Alzheimer’s disease. Journal of Cognitive Neuroscience, 12, 134–141.

    Article  PubMed  Google Scholar 

  • Bäckman, L., & Dixon, R. A. (1992). Psychological compensation: a theoretical framework. Psychological Bulletin, 112, 259–283.

    Article  PubMed  Google Scholar 

  • Bäckman, L., Lindenberger, U., Li, S.C., & Nyberg, L. (in press). Linking cognitive aging to alterations in dopaminergic neurotransmitter functioning: Recent data and future avenues. Neuroscience and Biobehavioral Reviews.

  • Bäckman, L., Nyberg, L., Lindenberger, U., Li, S. C., & Farde, L. (2006). The correlative triad among aging, dopamine, and cognition: current status and future prospects. Neuroscience and Biobehavioral Reviews, 30, 791–807.

    Article  PubMed  CAS  Google Scholar 

  • Bäckman, L., Small, B. J., & Wahlin, Å. (2001). Aging and memory: Cognitive and biological perspectives. In J. E. Birren & K. W. Schaie (Eds.), Handbook of the psychology of aging (5th ed., pp. 349–377). San Diego, CA: Academic.

    Google Scholar 

  • Beauchamp, M. H., Dagher, A., Panisset, M., & Doyon, J. (2008). Neural substrates of cognitive skill learning in Parkinson’s disease. Brain and Cognition, 68, 134–143.

    Article  CAS  PubMed  Google Scholar 

  • Bennett, I. J., Howard, J. H., Jr., & Howard, D. (2007). Age-Related differences in implicit learning of subtle third-order sequential structure. Journal of Gerontology: Psychological Sciences, 62B, 98–103.

    Google Scholar 

  • Berry, D. C. (1997). How implicit is implicit learning? Oxford: Oxford University Press.

    Google Scholar 

  • Berry, D. C., & Dienes, Z. (1993). Implicit learning: Theoretical and empirical issues. Hove, UK: Lawrence Erlbaum Associates.

    Google Scholar 

  • Brooks, D. N., & Baddeley, A. D. (1976). What can amnesic patients learn? Neuropsychologia, 14, 111–122.

    Article  CAS  PubMed  Google Scholar 

  • Cabeza, R. (2001). Cognitive neuroscience of aging: contributions of functional neuroimaging. Scandinavian Journal of Psychology, 42, 277–286.

    Article  CAS  PubMed  Google Scholar 

  • Cabeza, R., Anderson, N. D., Locantore, J. K., & McIntosh, A. R. (2002). Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage, 17, 1394–1402.

    Article  PubMed  Google Scholar 

  • Chang, Q., & Gold, P. E. (2003). Switching memory systems during learning: changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats. The Journal of Neuroscience, 23, 3001–3005.

    CAS  PubMed  Google Scholar 

  • Cherry, K. E., & Stadler, M. A. (1995). Implicit learning of a nonverbal sequence in younger and older adults. Psychology & Aging, 10, 379–394.

    Article  CAS  Google Scholar 

  • Cleeremans, A., Destrebecqz, A., & Boyer, M. (1998). Implicit learning: News from the front. Trends in Cognitive Sciences, 2, 406–416.

    Article  Google Scholar 

  • Cohen, N. J., Eichenbaum, H., DeAcedo, B. S., & Corkin, S. (1985). Different memory systems underlying acquisition of procedural and declarative knowledge. In D. S. Olton, E. Gamzu & S. Corkin (Eds.), Memory dysfunctions: An integration of animal and human research from preclinical and clinical perspectives (pp. 54–71). New York: New York Academy of Sciences.

    Google Scholar 

  • Cohen, N. J., Poldrack, R. A., & Eichenbaum, H. (1997). Memory for items and memory for relations in the procedural/declarative memory framework. Memory, 5, 131–178.

    Article  CAS  PubMed  Google Scholar 

  • Curran, T. (1997). Effects of aging on implicit sequence learning: accounting for sequence structure and explicit knowledge. Psychological Research, 60, 24–41.

    Article  CAS  PubMed  Google Scholar 

  • Curran, T., & Keele, S. W. (1993). Attentional and nonattentional forms of sequence learning. Journal of Experimental Psychology: Learning, Memory, and Cognition, 19, 189–202.

    Article  Google Scholar 

  • Daselaar, S. M., Rombouts, S. A. R. B., Veltman, D. J., Raaijmakers, J. G. W., & Jonker, C. (2003). Similar network activated by young and old adults during the acquisition of a motor sequence. Neurobiology of Aging, 24, 1013–1019.

    Article  PubMed  Google Scholar 

  • Davis, H. P., Klebe, K. J., Bever, B., & Spring, A. (1998). The effect of age on the learning of a nondeclarative category classification task. Experimental Aging Research, 24, 273–287.

    Article  CAS  PubMed  Google Scholar 

  • Dennis, N. A., Howard, J. H., Jr., & Howard, D. V. (2003). Age deficits in learning sequences of spoken words. Journal of Gerontology Series B: Psychological Sciences and Social Sciences, 58B, 224–227.

    Google Scholar 

  • Dennis, N. A., Howard, J. H., Jr., & Howard, D. V. (2006). Implicit sequence learning without motor sequencing in young and old adults. Experimental Brain Research, 175, 153–164.

    Article  Google Scholar 

  • D’Eredita, M. A., & Hoyer, W. J. (1999). An examination of the effects of adult age on explicit and implicit learning of figural sequences. Memory & Cognition, 27, 890–895.

    Google Scholar 

  • Dixon, R. A., Wahlin, Å., Maitland, S. B., Hultsch, D. F., Hertzog, C., & Bäckman, L. (2004). Episodic memory change in late adulthood: Generalizability across samples and performance indices. Memory & Cognition, 32, 768–778.

    Google Scholar 

  • Eichenbaum, H. (2000). A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience, 1, 41–50.

    Article  CAS  PubMed  Google Scholar 

  • Exner, C., Koschack, J., & Irle, E. (2002). The differential role of premotor frontal cortex and basal ganglia in motor sequence learning: evidence from focal basal ganglia lesions. Learning & Memory, 9, 376–386.

    Article  Google Scholar 

  • Feeney, J. J., Howard, J. H., Jr., & Howard, D. V. (2002). Implicit learning of higher order sequences in middle age. Psychology & Aging, 17, 351–355.

    Article  Google Scholar 

  • Fera, F., Weickert, T. W., Goldberg, T. E., Tessitore, A., Hariri, A., Das, S., et al. (2005). Neural mechanisms underlying probabilistic category learning in normal aging. Journal of Neuroscience, 25, 11340–11348.

    Article  CAS  PubMed  Google Scholar 

  • Fletcher, P. C., Zafiris, O., Frith, C. D., Honey, R. A. E., Corlett, P. R., Zilles, K., et al. (2005). On the benefits of not trying: Brain activity and connectivity reflecting the interactions of explicit and implicit sequence learning. Cerebral Cortex, 15, 1002–1015.

    Article  CAS  PubMed  Google Scholar 

  • Foerde, K., Knowlton, B. J., & Poldrack, R. A. (2006). Modulation of competing memory systems by distraction. Proceedings of the National Academy of Sciences, 103, 11778–11783.

    Article  CAS  Google Scholar 

  • Frensch, P. A. (1998). One concept, multiple meanings: On how to define the concept of implicit learning. In M. A. Stadler & P. A. Frensch (Eds.), Handbook of implicit learning (pp. 47–105). Thousand Oaks, CA: Sage.

    Google Scholar 

  • Frensch, P. A., & Miner, C. S. (1994). Effects of presentation rate and individual differences in short-term memory capacity on an indirect measure of serial learning. Memory & Cognition, 22, 95–110.

    CAS  Google Scholar 

  • Frensch, P. A., & Rünger, D. (2003). Implicit learning. Current Directions in Psychological Science, 12, 13–18.

    Article  Google Scholar 

  • Gabrieli, J. D. (1998). Cognitive neuroscience of human memory. Annual Review of Psychology, 49, 87–115.

    Article  CAS  PubMed  Google Scholar 

  • Gagnon, S., Bedard, M. J., & Turcotte, J. (2005). The effect of old age on supra-span learning of visuo-spatial sequences under incidental and intentional encoding instructions. Brain and Cognition, 59, 225–235.

    Article  PubMed  Google Scholar 

  • Gaillard, V., Arnaud, D., Michiels, S., & Cleeremans, A. (2009). Effects of age and practice in sequence learning: A graded account of ageing, learning, and control. European Journal of Cognitive Psychology., 21, 255–282.

    Article  Google Scholar 

  • Gaillard, V., Vandenberghe, M., Destrebecqz, A., & Cleeremans, A. (2006). First- and third-person approaches in implicit learning research. Consciousness and Cognition, 15, 709–722.

    Article  PubMed  Google Scholar 

  • Gluck, M. A., & Bower, G. H. (1988). From conditioning to category learning: an adaptive network model. Journal of Experimental Psychology: General, 117, 227–247.

    Article  CAS  Google Scholar 

  • Grafton, S. T., Hazeltine, E., & Ivry, R. B. (1998). Abstract and effector-specific representations of motor sequences identified with PET. Journal of Neuroscience, 18, 9420–9428.

    CAS  PubMed  Google Scholar 

  • Grieve, S. M., Clark, C. R., Williams, L. M., Peduto, A. J., & Gordon, E. (2005). Preservation of limbic and paralimbic structures in aging, 25, 391–401.

    Google Scholar 

  • Hackert, V. H., den Heijer, T., Oudkerk, M., Koudstaal, P. J., Hofman, A., & Breteler, M. M. B. (2002). Hippocampal head size associated with verbal memory performance in nondemented elderly. NeuroImage, 17, 1356–1372.

    Article  Google Scholar 

  • Harrington, D. L., & Haaland, K. Y. (1992). Skill learning in the elderly: diminished implicit and explicit memory for a motor sequence. Psychology & Aging, 7, 425–434.

    Article  CAS  Google Scholar 

  • Head, D., Raz, N., Gunning-Dixon, F., Williamson, A., & Acker, J. (2002). Age-Related differences in the course of cognitive skill acquisition: The role of regional cortical shrinkage and cognitive resources. Psychology and Aging, 17, 72–84.

    Article  PubMed  Google Scholar 

  • Head, D., Rodrigue, K. M., Kennedy, K. M., & Raz, N. (2008). Neuroanatomical and cognitive mediators of age-related differences in episodic memory. Neuropsychology, 22, 491–507.

    Article  PubMed  Google Scholar 

  • Heyes, C. M., & Foster, C. L. (2002). Motor learning by observation: evidence from a serial reaction time task. The Quarterly Journal of Experimental Psychology A: Human Experimental Psychology, 55, 593–607.

    CAS  PubMed  Google Scholar 

  • Hicks, L. H. (1964). Effects of overtraining on acquisition and reversal of place and response learning. Psychological Reports, 15, 49–462.

    Google Scholar 

  • Howard, D. V., & Howard, J. H., Jr. (1989). Age differences in learning serial patterns: direct versus indirect measures. Psychology and Aging, 4, 357–364.

    Article  CAS  PubMed  Google Scholar 

  • Howard, D. V., & Howard, J. H., Jr. (1992). Adult age differences in the rate of learning serial patterns: evidence from direct and indirect tests. Psychology and Aging, 7, 232–241.

    Article  CAS  PubMed  Google Scholar 

  • Howard, J. H., Jr., & Howard, D. V. (1997). Age differences in implicit learning of higher order dependencies in serial patterns. Psychology and Aging, 12, 634–656.

    Article  PubMed  Google Scholar 

  • Howard, D. V., & Howard, J. H., Jr. (2001). When it does hurt to try: Adult age differences in the effects of instructions on implicit pattern learning. Psychonomic Bulletin & Review, 8, 798–805.

    CAS  Google Scholar 

  • Howard, J. H., Jr., Howard, D. V., Dennis, N. A., & Kelly, A. J. (2008a). Implicit learning of predicitive relationships in three-element visual sequences by young and old adults. Journal of Experimental Psychology: Learning, Memory, and Cognition, 34, 1139–1157.

    Article  Google Scholar 

  • Howard, J. H., Jr., Howard, D. V., Dennis, N. A., LaVine, S., & Valentino, K. (2008b). Aging and implicit learning of an invariant association. Journal of Gerontology: Psychological Sciences, 63B, 100–105.

    Google Scholar 

  • Howard, J. H., Jr., Howard, D. V., Dennis, N. A., & Yankovich, H. (2007). Event timing and age deficits in higher-order sequence learning. Aging, Neuropsychology, and Cognition, 14, 1–22.

    Article  Google Scholar 

  • Howard, J. H., Jr., Howard, D. V., Dennis, N. A., Yankovich, H., & Vaidya, C. J. (2004a). Implicit spatial contextual learning in healthy aging. Neuropsychology, 18, 124–134.

    Article  Google Scholar 

  • Howard, D. V., Howard, J. H., Jr., Japikse, K., DiYanni, C., Thompson, A., & Somberg, R. (2004b). Implicit sequence learning: effects of level of structure, adult age, and extended practice. Psychology and Aging, 19, 79–92.

    Article  Google Scholar 

  • Hoyer, W. J., & Lincourt, A. E. (1998). Aging and the development of learning. In M. A. Stadler & P. A. Frensch (Eds.), Handbook of implicit learning (pp. 445–470). Thousand Oaks, CA: Sage.

    Google Scholar 

  • Jackson, G. M., Jackson, S. R., Harrison, J., Henderson, L., & Kennard, C. (1995). Serial reaction time learning and Parkinson’s disease: evidence for a procedural learning deficit. Neuropsychologia, 33, 577–593.

    Article  CAS  PubMed  Google Scholar 

  • Jimenez, L. (2008). Taking patterns for chunks: Is there any evidence of chunk learning in continuous serial reaction-time tasks? Psychological Research, 71, 387–396.

    Article  Google Scholar 

  • Kelly, S. W., & Burton, A. M. (2001). Learning complex sequences: No role for observation? Psychological Research, 65, 15–23.

    Article  CAS  PubMed  Google Scholar 

  • Kemper, T. L. (1994). Neuroanatomical and neuropathological changes during aging and dementia. In M. L. Albert & J. E. Knoefel (Eds.), Clinical Neurology of Aging (2nd ed., pp. 3–67). New York: Oxford University Press.

    Google Scholar 

  • Kemps, E., & Newson, R. (2006). Comparison of adult age differences in verbal and visuo-spatial memory: the importance of ‘pure’, parallel and validated measures. Journal of Clinical and Experimental Neuropsychology, 28, 341–356.

    Article  PubMed  Google Scholar 

  • Knopman, D., & Nissen, M. J. (1991). Procedural learning is impaired in Huntington’s disease: evidence from the serial reaction time task. Neuropsychologia, 29, 245–254.

    Article  CAS  PubMed  Google Scholar 

  • Knowlton, B. J., Mangels, J. A., & Squire, L. R. (1996). A neostriatal habit learning system in humans. Science, 273, 1399–1402.

    Article  CAS  PubMed  Google Scholar 

  • Kreitzer, A. C., & Malenka, R. C. (2007). Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson’s disease models. Nature, 445, 643–647.

    Article  CAS  PubMed  Google Scholar 

  • Langley, L. K., & Madden, D. J. (2000). Functional neuroimaging of memory: implications for cognitive aging. Microscopy Research and Technique, 51, 75–84.

    Article  CAS  PubMed  Google Scholar 

  • Lee, A. S., Duman, R. S., & Pittenger, C. (2008). A double dissociation revealing bidirectional competition between striatum and hippocampus during learning. Proceedings of the National Academy of Sciences of the United States of America, 105, 17163–17168.

    Article  CAS  PubMed  Google Scholar 

  • Lieberman, M. D., Chang, G. Y., Chiao, J., Bookheimer, S. Y., & Knowlton, B. J. (2004). An event-related fMRI study of artificial grammar learning in a balanced chunk strength design. Journal of Cognitive Neuroscience, 16, 427–438.

    Article  PubMed  Google Scholar 

  • Locascio, J. J., Corkin, S., & Growdon, J. H. (2003). Relation between clinical characteristics of Parkinson’s disease and cognitive decline. Journal of Clinical and Experimental Neuropsychology, 25, 94–109.

    Article  PubMed  Google Scholar 

  • Lungu, O. V., Wächter, T., Liu, T., Willinghamn, D. T., & Ashe, J. (2004). Probability detection mechanisms and motor learning. Experimental Brain Research, 159, 135–150.

    Article  CAS  Google Scholar 

  • Merikle, P. M., & Daneman, M. (1996). Memory for unconsciously perceived events: evidence from anesthetized patients. Consciousness and Cognition, 5, 525–541.

    Article  CAS  PubMed  Google Scholar 

  • Meulemans, T., & Van Der Linden, M. (1997). Does the artificial grammar learning paradigm involve the acquisition of complex information? Psychologica Belgica, 37, 69–88.

    Google Scholar 

  • Meulemans, T., Van Der Linden, M., & Perruchet, P. (1998). Implicit sequence learning in children. Journal of Experimental Child Psychology, 69, 199–221.

    Article  CAS  PubMed  Google Scholar 

  • Midford, R., & Kirsner, K. (2005). Implicit and explicit learning in aged and young adults. Aging, Neuropsychology, and Cognition, 12, 359–387.

    Article  Google Scholar 

  • Miller, A. K. H., Alston, R. L., & Corselllis, J. A. N. (1980). Variation with age in the volumes of grey and white matter in the cerebral hemispheres. Neuropathology & Applied Neurobiology, 6, 119–132.

    Article  CAS  Google Scholar 

  • Moody, T. D., Bookheimer, S. Y., Vanek, Z., & Knowlton, B. J. (2004). An implicit learning task activates medial temporal lobe in patients with Parkinson’s disease. Behavioral Neuroscience, 118, 438–442.

    Article  PubMed  Google Scholar 

  • Myerson, J., Hale, S., Rhee, S. H., & Jenkins, L. (1999). Selective interference with verbal and spatial working memory in young and older adults. Journal of Gerontology Series B: Psychological Sciences and Social Sciences, 54B, 161–164.

    Google Scholar 

  • Negash, S., Howard, D. V., Japikse, K. C., & Howard, J. H., Jr. (2003). Age-related differences in implicit learning of non-spatial sequences. Aging, Neuropsychology and Cognition, 10, 108–121.

    Article  Google Scholar 

  • Nejati, V., Garusi Farshi, M. T., Ashayeri, H., & Aghdasi, M. T. (2008). Dual task interference in implicit sequence learning by young and old adults. International Journal of Geriatric Psychiatry, 23, 801–804.

    Article  CAS  PubMed  Google Scholar 

  • Nissen, M. J., & Bullemer, P. T. (1987). Attentional requirements for learning: Evidence from performance measures. Cognitive Psychology, 19, 1–32.

    Article  Google Scholar 

  • Nyberg, L., Maitland, S. B., Rönnlund, M., Bäckman, L., Dixon, R. A., Wahlin, Å., et al. (2003). Selective adult age differences in an age-invariant multi-factor model of declarative memory. Psychology and Aging, 18, 149–160.

    Article  PubMed  Google Scholar 

  • Packard, M. G. (1999). Glutamate infused post-training into the hippocampus or caudate-putamen differentially strengthens place and response learning. Proceedings of the National Academy of Sciences of the United States of America, 93, 8683–8687.

    Google Scholar 

  • Packard, M. G. (2009). Exhumed from thought: Basal ganglia and response learning in the plus-maze. Behavioral Brain Research, 199, 24–31.

    Article  Google Scholar 

  • Packard, M. G., & Knowlton, B. J. (2002). Learning and memory functions of the basal ganglia. Annual Review of Neuroscience, 25, 563–593.

    Article  CAS  PubMed  Google Scholar 

  • Packard, M. G., & McGaugh, J. L. (1996). Inactivation of the hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory, 65, 65–72.

    Article  CAS  PubMed  Google Scholar 

  • Park, D. C. (2000). The basic mechanisms accounting for age-related decline in cognitive function. In D. C. Park & N. Schwarz (Eds.), Cognitive aging: A primer Vol. 11 (pp. 3–19). Philadelphia: Psychology Press.

    Google Scholar 

  • Perruchet, P., & Pacton, S. (2006). Implicit learning and statistical learning: one phenomenon, two approaches. Trends in Cognitive Sciences, 10, 233–238.

    Article  PubMed  Google Scholar 

  • Persson, J., Nyberg, L., Lind, J., Larsson, A., Nilsson, L. H., Ingvar, M., et al. (2006). Structure-function correlates of cognitive decline in aging. Cerebral Cortex, 16, 907–815.

    Article  PubMed  Google Scholar 

  • Poldrack, R. A., Clark, J., Pare-Blagoev, E. J., Shohamy, D., Creso Moyano, J., Myers, C., et al. (2001). Interactive memory systems in the human brain. Nature, 414, 546–550.

    Article  CAS  PubMed  Google Scholar 

  • Poldrack, R. A., Prabhakaran, V., Seger, C. A., & Gabrieli, J. D. (1999). Striatal activation during acquisition of a cognitive skill. Neuropsychology, 13, 564–574.

    Article  CAS  PubMed  Google Scholar 

  • Poldrack, R. A., & Rodriguez, P. (2004). How do memory systems interact? Evidence from human classification learning. Neurobiology of Learning and Memory, 82, 324–332.

    Article  PubMed  Google Scholar 

  • Price, A. L. (2005). Cortico-striatal contributions to category learning: dissociating the verbal and implicit systems. Behavorial Neuroscience, 119, 1438–1447.

    Article  Google Scholar 

  • Prull, M. W., Gabrieli, J. D. E., & Bunge, S. A. (2000). Age-related changes in memory: A cognitive neuroscience perspective. In F. I. M. Craik & T. A. Salthouse (Eds.), Handbook of aging and cognition (2nd ed., pp. 91–153). Mahwah: Erlbaum.

    Google Scholar 

  • Rajah, M. N., & D'Esposito, M. (2005). Region-specific changes in prefrontal function with age: a review of PET and fMRI studies on working and episodic memory. Brain, 128, 1964–1983.

    Article  PubMed  Google Scholar 

  • Rakshi, J. S., Uema, T., Ito, K., Bailey, D. L., Morrish, P. K., Ashburner, J., et al. (1999). Frontal, midbrain and striatal dopaminergic function in early and advanced Parkinson's disease A 3D [(18)F]dopa-PET study. Brain, 122, 1637–1650.

    Article  PubMed  Google Scholar 

  • Rauch, S. L., Wedig, M. M., Wright, C. I., Martis, B., McMullin, K. G., Shin, L. M., et al. (2007). Functional magnetic resonance imaging study of regional brain activation during implicit sequence learning in obsessive-compulsive disorder. Biological Psychiatry, 61, 330–336.

    Article  PubMed  Google Scholar 

  • Rauch, S. L., Whalen, P. J., Savage, C. R., Curran, T., Kendrick, A., Brown, H. D., et al. (1997). Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging. Human Brain Mapping, 5, 124–132.

    Article  CAS  PubMed  Google Scholar 

  • Rausch, R., & Ary, C. M. (1990). Supraspan learning in patients with unilateral anterior temporal lobe resections. Neuropsychologia, 28, 111–120.

    Article  CAS  PubMed  Google Scholar 

  • Raz, N., Lindenberger, U., Rodrigue, K. M., Kennedy, K. M., Head, D., Williamson, A., et al. (2005). Regional brain changes in aging healthy adults: General trends, individual differences and modifiers. Cerebral Cortex, 15, 1676–1689.

    Article  PubMed  Google Scholar 

  • Raz, N., Rodrigue, K. M., Kennedy, K. M., Head, D., Gunning-Dixon, F., & Acker, J. D. (2003). Differential aging of the human striatum: longitudinal evidence. American Journal of Neuroradiology, 24, 1849–1856.

    PubMed  Google Scholar 

  • Reber, A. S. (1967). Implicit learning of artificial grammars. Journal of Verbal Learning and Verbal Behavior, 6, 855–863.

    Article  Google Scholar 

  • Reber, A. S. (1989). Implicit learning and tacit knowledge. Journal of Experimental Psychology: General, 118, 219–235.

    Article  Google Scholar 

  • Reber, P. J., Knowlton, B. J., & Squire, L. R. (1996). Dissociable properties of memory systems: Differences in the flexibility of declarative and nondeclarative knowledge. Behavioral Neuroscience, 110, 861–871.

    Article  CAS  PubMed  Google Scholar 

  • Reber, A. S., & Kotovsky, K. (1992, July). Learning and problem solving under a memory load. Paper presented at the Fourteenth Annual Conference of the Cognitive Science Society, Bloomington, Indiana

  • Reber, P. J., & Squire, L. R. (1994). Parallel brain systems for learning with and without awareness. Learning & Memory, 1, 217–229.

    CAS  Google Scholar 

  • Rieckmann, A., & Fischer, H. (2009). & Bäckman, L. Activation in striatum and medial-temporal lobe during implicit learning in younger and older adults: Relations to performance. Manuscript submitted for publication.

    Google Scholar 

  • Robertson, E. M., & Pascual-Leone, A. (2001). Aspects of sensory guidance in sequence learning. Experimental Brain Research, 137, 336–345.

    Article  CAS  Google Scholar 

  • Rose, M., Haider, H., Weiller, C., & Büchel, C. (2002). The role of the medial temporal lobe structures in implicit learning: An event-related fMRI study. Neuron, 36, 1221–1231.

    Article  CAS  PubMed  Google Scholar 

  • Salthouse, T. A. (1995). Differential age-related influences on memory for verbal-symbolic information and visual-spatial information? Journal of Gerontology: Psychological Sciences, 50B, 193–201.

    Google Scholar 

  • Salthouse, T. A., McGuthry, K. E., & Hambrick, D. Z. (1999). A framework for analyzing and interpreting differential aging patterns: Application to three measures of implicit learning. Aging, Neuropsychology and Cognition, 6, 1–18.

    Article  Google Scholar 

  • Schacter, D. L. (1987). Implicit expressions of memory in organic amnesia: learning of new facts and associations. Human Neurobiology, 6, 107–118.

    CAS  PubMed  Google Scholar 

  • Schendan, H. E., Searl, M. M., Melrose, R. J., & Stern, C. E. (2003). An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron, 37, 1013–1025.

    Article  CAS  PubMed  Google Scholar 

  • Schmitter-Edgecombe, M., & Nissley, H. M. (2002). Effects of aging on implicit covariation learning. Aging, Neuropsychology and Cognition, 9, 61–75.

    Article  Google Scholar 

  • Schugens, M. M., Daum, I., Spindler, M., & Birbaumer, N. (1997). Differential effects of aging on explicit and implicit memory. Aging, Neuropsychology, and Cognition, 4, 33–44.

    Article  Google Scholar 

  • Seger, C. A. (1994). Implicit learning. Psychological Bulletin, 115, 163–196.

    Article  CAS  PubMed  Google Scholar 

  • Seger, C. A., & Cincotta, C. M. (2006). Dynamics of frontal, striatal, and hippocampal systems during rule learning. Cerebral Cortex, 16, 1546–1555.

    Article  PubMed  Google Scholar 

  • Seidler, R. D. (2006). Differential effects of age on sequence learning and sensorimotor adaptation. Brain Research Bulletin, 70, 337–346.

    Article  PubMed  Google Scholar 

  • Shanks, D. R., & St. John, M. F. (1994). Characteristics of dissociable human learning systems. Behavioral and Brain Sciences, 17, 367–447.

    Article  Google Scholar 

  • Shea, C. H., Park, J. H., & Braden, H. W. (2006). Age-related effects in sequential motor learning. Physical Therapy, 86, 478–488.

    PubMed  Google Scholar 

  • Shohamy, D., Myers, C. S., Kalanithi, J., & Gluck, M. A. (2008). Basal ganglia and dopamine contributions to probabilistic category learning. Neuroscience & Biobehavioral Reviews, 32, 219–236.

    Article  CAS  Google Scholar 

  • Smith, J. G., & McDowall, J. (2004). Impaired higher-order implicit sequence learning on the verbal version of the serial reaction time task in patients with Parkinson's disease. Neuropsychology, 18, 679–691.

    Article  PubMed  Google Scholar 

  • Smith, J. G., & McDowall, J. (2006). The implicit learning deficit in patients with Parkinson´s disease: A matter of impaired sequence integration ? Neuropsychologica, 44, 275–288.

    Article  Google Scholar 

  • Smith, J. G., Siegert, R., & McDowall, J. (2001). Preserved implicit learning on both the serial reaction time task and artificial grammar in patients with Parkinson’s disease. Brain and Cognition, 45, 378–391.

    Article  CAS  PubMed  Google Scholar 

  • Song, S., Howard, J. H., Jr., & Howard, D. V. (2007). Implicit probabilistic sequence learning is independent of explicit awareness. Learning and Memory, 14, 167–176.

    Article  PubMed  Google Scholar 

  • Song, S., Howard, J. H., Jr., & Howard, D. V. (2008). Perceptual sequence learning in a serial reaction time task. Experimental Brain Research, 189, 145–58.

    Article  Google Scholar 

  • Song, S., Marks, B., Howard, J. H., Jr., & Howard, D. V. (2009). Evidence for parallel explicit and implicit sequence learning systems in older adults. Behavioral Brain Research, 196, 328–332.

    Article  Google Scholar 

  • Squire, L. R., & Frambach, M. (1990). Cognitive skill learning in amnesia. Psychobiology, 18, 109–117.

    Google Scholar 

  • Squire, L. R., Knowlton, B., & Musen, G. (1993). The structure and organization of memory. Annual Review of Psychology, 44, 453–495.

    Article  CAS  PubMed  Google Scholar 

  • Squire, L. R., Ojemann, J. G., Miezin, F. M., Petersen, S. E., Videen, T. O., & Raichle, M. E. (1992). Activation of the hippocampus in normal humans: a functional anatomical study of memory. Proceedings of the National Academy of Sciences USA, 89, 1837–1841.

    Article  CAS  Google Scholar 

  • Squire, L. R., & Zola, S. M. (1996). Structure and function of declarative and nondeclarative memory systems. Proceedings of the National Academy of Sciences USA, 93, 13515–13522.

    Article  CAS  Google Scholar 

  • Turcotte, J., Gagnon, S., & Poirier, M. (2005). The effect of old age on the learning of supraspan sequences. Psychology and Aging, 20, 251–260.

    Article  PubMed  Google Scholar 

  • Verhaeghen, P., Marcoen, A., & Goossens, L. (1993). Facts and fiction about memory aging: A quantitative integration of research findings. Journal of Gerontology: Psychological Sciences, 48B, 157–171.

    Google Scholar 

  • Voermans, N. C., Petersson, K. M., Daudey, L., Weber, B., Van Spaendonck, K. P., Kremer, H. P., et al. (2004). Interaction between the human hippocampus and the caudate nucleus during route recognition. Neuron, 43, 427–435.

    Article  CAS  PubMed  Google Scholar 

  • Werheid, K., Zysset, S., Muller, A., Reuter, M., & von Cramon, D. Y. (2003). Rule learning in a serial reaction time task: an fMRI study on patients with early Parkinson's disease. Cognitive Brain Research, 16, 273–284.

    Article  PubMed  Google Scholar 

  • Willingham, D. B. (1999). Implicit motor sequence learning is not purely perceptual. Memory & Cognition, 27, 561–572.

    CAS  Google Scholar 

  • Willingham, D. D., & Goedert-Eschman, K. (1999). The relation between implicit and explicit learning: Evidence for parallel development. Psychological Science, 10, 531–534.

    Article  Google Scholar 

  • Willingham, D. B., & Koroshetz, W. J. (1993). Evidence for dissociable motor skills in Huntington’s disease patients. Psychobiology, 21, 173–182.

    Google Scholar 

  • Willingham, D., Koroshetz, W., & Peterson, E. (1996). Motor skills have diverse neural bases: Spared and impaired skill acquisition in Huntington's disease. Neuropsychology, 10, 315–321.

    Article  Google Scholar 

  • Willingham, D. B., Nissen, M. J., & Bullemer, P. (1989). On the development of procedural knowledge. Journal of Experimental Psychology: Learning, Memory, & Cognition, 15, 1047–1060.

    Article  CAS  Google Scholar 

  • Willingham, D. B., & Preuss, L. (1995). The death of implicit memory. Psyche, 2, 1–10.

    Google Scholar 

  • Willingham, D. B., Salidis, J., & Gabrieli, J. D. E. (2002). Direct comparison of neural systems mediating conscious and unconscious skill learning. Journal of Neurophysiology, 88, 1451–1460.

    PubMed  Google Scholar 

  • Zacks, R. T., Hasher, L., & Li, K. Z. H. (2000). Human Memory. In T. A. Salthouse & F. I. M. Craik (Eds.), Handbook of aging and cognition (2nd ed., pp. 293–357). Mahwah: Erlbaum.

    Google Scholar 

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Acknowledgements

Preparation of this article was supported by grants from the Swedish Research Council and Swedish Brain Power, and an Alexander von Humboldt Research Award to Lars Bäckman, and a studentship from the Leverhulme Trust to Anna Rieckmann.

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Rieckmann, A., Bäckman, L. Implicit Learning in Aging: Extant Patterns and New Directions. Neuropsychol Rev 19, 490–503 (2009). https://doi.org/10.1007/s11065-009-9117-y

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