Skip to main content

Extensive stimulus repetition leads older adults to show delayed functional magnetic resonance imaging adaptation

Brain Imaging and Behavior volume 6, pages 357–365 (2012)Cite this article

Abstract

We investigated whether extensive repetition can diminish age-related differences between younger and older adults in functional magnetic resonance adaptation (fMR-A). Datasets were obtained from 26 younger and 24 older healthy adults presented with two scenes that repeated 20 times amongst other novel scenes during fMRI scanning. The average cortical responses to the first eight (Repetitions 1-7) and the last eight (Repetitions 12-19) presentations out of 20 were compared within each group. Younger adults showed similar levels of fMR-A in both repetition sets. Conversely, older adults did not show reliable fMR-A in Repetitions 1-7, but they did in Repetitions 12-19; subtracting the latter from the former revealed a significant effect within left inferior occipital, left lingual, and the posterior part of fusiform gyrus. We concluded that cortical responsiveness in older adults are compromised, but extensive repetition can lead older adults to show a delayed but closer level of fMR-A compared to younger adults.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

References

  • Begleiter, H., Porjesz, B., & Wang, W. (1993). A neurophysiologic correlate of visual short-term memory in humans. Electroencephalography and Clinical Neurophysiology, 87, 46–53.

    PubMed  Article  CAS  Google Scholar 

  • Bergerbest, D., Gabrieli, J. D. E., Whitfield-Gabrieli, S., Kim, H., Stebbins, G. T., Bennett, D. A., & Fleichman, D. A. (2009). Age-associated reduction of asymmetry in prefrontal function and preservation of conceptual repetition priming. Neuroimage, 45, 237–246.

    PubMed  Article  CAS  Google Scholar 

  • Binder, J. R., Bellgowan, P. S. F., Hammeke, T. A., Possing, E. T., & Frost, J. A. (2005). A comparison of two fMRI protocols for eliciting hippocampal activation. Epilepsia, 46, 1061–1070.

    PubMed  Article  Google Scholar 

  • Brett, M., Anton, J-L., Valabregue, R., Poline, J-B. (2002). Region of interest analysis using an SPM toolbox [abstract] Presented at the 8th International Conference on Functional Mapping of the Human Brain, June 2–6, 2002, Sendai, Japan. NeuroImage 16, 2.

  • Burke, S. N., & Barnes, C. A. (2006). Neural plasticity in the ageing brain. Nature Reviews Neuroscience, 7, 30–40.

    PubMed  Article  CAS  Google Scholar 

  • Chee, M. W. L., Goh, J. O. S., Venkatraman, V., Tan, J. C., Gutchess, A., Sutton, B., Hebrank, A., Leshikar, E., & Park, D. (2006). Age-related changes in object processing and contextual binding revealed using fMR adaptation. Journal of Cognitive Neuroscience, 18, 495–507.

    PubMed  Article  Google Scholar 

  • Connelly, S. L., Hasher, L., & Zacks, R. T. (1991). Age and reading: the impact of distraction. Psychology and Aging, 6, 533–541.

    PubMed  Article  CAS  Google Scholar 

  • D’Esposito, M., Deouell, L., & Gazzaley, A. (2003). Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nature Reviews Neuroscience, 4, 1–10.

    Google Scholar 

  • Dale Stevens, W., Hasher, L., Chiew, K. S., & Grady, C. L. (2008). A neural mechanism underlying memory failure in older adults. Journal of Neuroscience, 26, 12820–12824.

    Article  Google Scholar 

  • Desimone, R. (1996). Neural mechanisms for visual memory and their role in attention. Proceedings of the National Academy of Sciences of the United States of America, 93, 13494–13499.

    PubMed  Article  CAS  Google Scholar 

  • Epstein, R., & Kanwisher, N. (1998). A cortical representation of the local visual environment. Nature, 392, 598–601.

    PubMed  Article  CAS  Google Scholar 

  • Epstein, R. A., Higgins, J. S., & Thompson-Schill, S. L. (2005). Learning places from views: Variation in scene processing as a function of experience and navigational ability. Journal of Cognitive Neuroscience, 17, 73–83.

    Google Scholar 

  • 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, 189–198.

    PubMed  Article  CAS  Google Scholar 

  • Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J. P., Frith, C. D., & Frackowiak, R. S. J. (1995). Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapping, 2, 189–210.

    Article  Google Scholar 

  • Goh, J. O., Chee, M. W., Tan, J. C., Venkatraman, V., Hebrank, A., Leshikar, E. D., Jenkins, L., Sutton, P. B., Gutchess, A. H., & Park, D. C. (2007). Age and culture modulate object processing and object-scene binding in the ventral visual area. Cognitive, Affective, and Behavioral Neuroscience, 7, 44–52.

    Article  Google Scholar 

  • Goh, J. O., Suzuki, A., & Park, D. C. (2010). Reduced neural selectivity increases fMRI adaptation with age during face discrimination. NeuroImage, 51, 336–344.

    PubMed  Article  Google Scholar 

  • Golby, A. J., Poldrack, R. A., Brewer, J. B., Spencer, D., Desmond, J. E., Aron, A. P., & Gabrieli, J. D. E. (2001). Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. Brain, 124, 1841–1854.

    PubMed  Article  CAS  Google Scholar 

  • Grady, C. L. (2008). Cognitive neuroscience of aging. Annals of the New York Academy of Sciences, 1124, 127–144.

    PubMed  Article  Google Scholar 

  • Grady, C. L., Yu, H., & Alain, C. (2008). Age-related differences in brain activity underlying working memory for spatial and nonspatial auditory information. Cerebral Cortex, 18, 189–199.

    PubMed  Article  Google Scholar 

  • Grady, C. L., Charlton, R., He, Y., & Alain, C. (2011). Age differences in fMRI adaptation for sound identity and location. Frontiers in Human Neuroscience, 5, 1–12.

    Article  Google Scholar 

  • Grill-Spector, K., & Malach, R. (2001). fMR-adaptation: a tool for studying the functional properties of human cortical neurons. Acta Psychologia, 107, 293–321.

    Article  CAS  Google Scholar 

  • Grill-Spector, K., Kushnir, T., Edelman, S., Avidan, G., Itzchak, Y., & Malach, R. (1999). Differential processing of objects under various viewing conditions in the human lateral occipital cortex. Neuron, 24, 187–203.

    PubMed  Article  CAS  Google Scholar 

  • Grill-Spector, K., Henson, R., & Martin, A. (2006). Repetition and the brain: neural models of stimulus-specific effects. Trends in Cognitive Sciences, 10, 14–23.

    PubMed  Article  Google Scholar 

  • Grill-Spector, K., Golarai, G., & Gabrieli, J. (2008). Developmental neuroimaging of the human ventral visual cortex. Trends in Cognitive Sciences, 12, 152–162.

    PubMed  Article  Google Scholar 

  • Healey, M. K., Campbell, K. L., & Hasher, L. (2008). Cognitive aging and increased distractibility: costs and potential benefits. Progress in Brain Research, 169, 353–363.

    PubMed  Article  Google Scholar 

  • Lancaster, J. L., Summerln, J. L., Rainey, L., Freitas, C. S., & Fox, P. T. (1997). The Talairach Daemon, a database server for Talairach Atlas Labels. NeuroImage, 5, S633.

    Google Scholar 

  • Lancaster, J. L., Woldorff, M. G., Parsons, L. M., Liotti, M., Freitas, C. S., Rainey, L., Kochunov, P. B., Nickerson, D., Mikiten, S. A., & Fox, P. T. (2000). Automated Talairach atlas labels for functional brain mapping. Human Brain Mapping, 10, 120–131.

    PubMed  Article  CAS  Google Scholar 

  • Lee, Y., Grady, C. L., Habak, C., Wilson, H. R., & Moscovitch, M. (2011). Face processing changes in normal aging revealed by fMRI adaptation. Journal of Cognitive Neuroscience, 23, 3433–3447.

    PubMed  Article  Google Scholar 

  • Maldjian, J. A., Laurienti, P. J., Burdette, J. B., & Kraft, R. A. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage, 19, 1233–1239.

    PubMed  Article  Google Scholar 

  • Maldjian, J. A., Laurienti, P. J., & Burdette, J. B. (2004). Precentral gyrus discrepancy in electronic versions of the Talairach Atlas. Neuroimage, 21, 450–455.

    PubMed  Article  Google Scholar 

  • Murray, S. O., & Wojciulik, E. (2004). Attention increases neural selectivity in the human lateral occipital complex. Nature Neuroscience, 7, 70–74.

    Google Scholar 

  • Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia, 9, 97–113.

    PubMed  Article  CAS  Google Scholar 

  • Park, D. C., & Reuter-Lorenz, P. (2009). The adaptive brain: aging and neurocognitive scaffolding. Annual Review of Psychology, 60, 173–96.

    PubMed  Article  Google Scholar 

  • Rand-Giovannetti, E. R., Chua, E. F., Driscoll, A. E., Schacter, D. L., Albert, M. S., & Sperling, R. A. (2006). Hippocampal and neocortical activation during repetitive encoding in older persons. Neurobiology of Aging, 27, 173–182.

    PubMed  Article  Google Scholar 

  • Rosenzweig, E. S., Rao, G., McNaughton, B. L., & Barnes, C. A. (1997). Role of temporal summation in age-related long-term potentiation-induced deficits. Hippocampus, 7, 549–558.

    PubMed  Article  CAS  Google Scholar 

  • Sawamura, H., Orban, G. A., & Vogels, R. (2006). Selectivity of neuronal adaptation does not match response selectivity: a single-cell study of the fMRI adaptation paradigm. Neuron, 49, 307–318.

    PubMed  Article  CAS  Google Scholar 

  • Schmitz, T. W., Cheng, F. H., & De Rosa, E. (2010). Failing to ignore: paradoxical neural effects of perceptual load on early attentional selection in normal aging. The Journal of Neuroscience, 30, 14750–14758.

    PubMed  Article  CAS  Google Scholar 

  • Schweinberger, S. R., Pfütze, E.-M., & Sommer, W. (1995). Repetition priming and associative priming of face recognition: evidence from event-related potentials. Journal of Experimental Psychology: Learning, Memory, and Cognition, 21, 722–736.

    Article  Google Scholar 

  • Sperling, R. (2007). Functional MRI studies of associative encoding in normal aging, mild cognitive impairment, and Alzheimer's disease. Annals of New York Academy of Sciences, 1097, 146–155.

    Article  Google Scholar 

  • Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage, 15, 273–289.

    PubMed  Article  CAS  Google Scholar 

  • Wiggs, C. L., & Martin, A. (1998). Properties and mechanisms of perceptual priming. Current Opinion in Neurobiology, 8, 227–233.

    PubMed  Article  CAS  Google Scholar 

  • Xiang, J. Z., & Brown, M. W. (1998). Differential neuronal encoding of novelty, amiliarity and recency in regions of the anterior temporal lobe. Neuropharmacology, 37, 657–676.

    PubMed  Article  CAS  Google Scholar 

  • Yi, D.-J., & Chun, M. M. (2005). Attentional modulation of learning-related repetition attenuation effects in human parahippocampal cortex. The Journal of Neuroscience, 25, 3593–3600.

    Google Scholar 

Download references

Acknowledgements

This study was supported by Grant-in-Aid for Young Scientists (B) 21791162 and Grant-in-Aid for Scientific Research (B) 21300196 by the Ministry of Education, Science, Sports and Culture, Japan and AcRF Tier 1, Ministry of Education, Singapore. We thank Toyota Home for permission to use pictures of their model homes for experimental stimuli, Tarik Bel-Bahar for editing English, and Yukari Ojima for supporting data collection.

Author information

Affiliations

  1. Neuroimaging and Informatics Lab, Department of Gerontechnology, National Center for Geriatrics and Gerontology, Ohbu, Aichi, Japan

    Makoto Miyakoshi & Toshiharu Nakai

  2. Division of Psychology, School of Humanities and Social Sciences, Nanyang Technological University, Singapore, Singapore

    S.-H. Annabel Chen & Chiao-Yi Wu

  3. Center for Optoelectronic Biomedicine, National Taiwan University College of Medicine, Taipei, Taiwan

    Kayako Matsuo

  4. Department of Social and Human Environment, Graduate School of Environmental Studies, Nagoya University, Nagoya, Aichi, Japan

    Atsunobu Suzuki

Authors
  1. Makoto Miyakoshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S.-H. Annabel Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kayako Matsuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chiao-Yi Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Atsunobu Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Toshiharu Nakai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Makoto Miyakoshi.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Miyakoshi, M., Chen, SH.A., Matsuo, K. et al. Extensive stimulus repetition leads older adults to show delayed functional magnetic resonance imaging adaptation. Brain Imaging and Behavior 6, 357–365 (2012). https://doi.org/10.1007/s11682-012-9148-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-012-9148-5

Keywords

  • Aging
  • fMRI
  • Adaptation
  • Repetition suppression
  • Scene recognition
  • Parahippocampus