Compensation through increased functional connectivity: Neural correlates of inhibition in old and young
Pages 2057 - 2069
Abstract
With increasing age, people experience more difficulties with suppressing irrelevant information, which may have a major impact on cognitive functioning. The extent of decline of inhibitory functions with age is highly variable between individuals. In this study, we used ERPs and phase locking analyses to investigate neural correlates of this variability in inhibition between individuals. Older and younger participants performed a selective attention task in which relevant and irrelevant information was presented simultaneously. The participants were split into high and low performers based on their level of inhibition inefficiency, that is, the slowing of RTs induced by information that participants were instructed to ignore. P1 peak amplitudes were larger in low performers than in high performers, indicating that low performers were less able to suppress the processing of irrelevant stimuli. Phase locking analyses were used as a measure of functional connectivity. Efficient inhibition in both age groups was related to the increased functional connectivity in the alpha band between frontal and occipito-parietal ROIs in the prestimulus interval. In addition, increased power in the alpha band in occipito-parietal ROIs was related to better inhibition both before and after stimulus onset. Phase locking in the upper beta band before and during stimulus presentation between frontal and occipito-parietal ROIs was related to a better performance in older participants only, suggesting that this is an active compensation mechanism employed to maintain adequate performance. In addition, increased top-down modulation and increased power in the alpha band appears to be a general mechanism facilitating inhibition in both age groups.
References
[1]
Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2004). Inhibition and the right inferior frontal cortex. Trends in Cognitive Sciences, 8, 170-177.
[2]
Buschman, T. J., & Miller, E. K. (2007). Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science, 315, 1860-1864.
[3]
Cabeza, R. (2002). Hemispheric asymmetry reduction in older adults: The HAROLD model. Psychology and Aging, 17, 85-100.
[4]
Caparos, S., & Linnell, K. J. (2010). The spatial focus of attention is controlled at perceptual and cognitive levels. Journal of Experimental Psychology: Human Perception and Performance, 36, 1080-1107.
[5]
Colcombe, S. J., Kramer, A. F., Erickson, K. I., & Scalf, P. (2005). The implications of cortical recruitment and brain morphology for individual differences in inhibitory function in aging humans. Psychology & Aging, 20, 363-375.
[6]
Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3, 201-215.
[7]
Daffner, K. R., Sun, X., Tarbi, E. C., Rentz, D. M., Holcomb, P. J., & Riis, J. L. (2011). Does compensatory neural activity survive old-old age? Neuroimage, 54, 427-438.
[8]
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, 1201-1209.
[9]
de Fockert, J. W., Ramchurn, A., van Velzen, J., Bergström, Z., & Bunce, D. (2009). Behavioral and ERP evidence of greater distractor processing in old age. Brain Research, 1282, 67-73.
[10]
Duverne, S., Motamedinia, S., & Rugg, M. D. (2008). The relationship between aging, performance, and the neural correlates of successful memory encoding. Cerebral Cortex, 19, 733-744.
[11]
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.
[12]
Freunberger, R., Höller, Y., Griesmayr, B., Gruber, W., Sauseng, P., & Klimesch, W. (2008). Functional similarities between the P1 component and alpha oscillations. European Journal of Neuroscience, 27, 2330-2340.
[13]
Fries, P. (2005). A mechanism for cognitive dynamics: Neuronal communication through neuronal coherence. Trends in Cognitive Sciences, 9, 474-480.
[14]
Gazzaley, A., Clapp, W., Kelley, J., McEvoy, K., Knight, R. T., & D'Esposito, M. (2008). Age-related top-down suppression deficit in the early stages of cortical visual memory processing. Proceedings of the National Academy of Sciences, U.S.A., 105, 13122-13126.
[15]
Gazzaley, A., Cooney, J. W., McEvoy, K., Knight, R. T., & D'Esposito, M. (2005). Top-down enhancement and suppression of the magnitude and speed of neural activity. Journal of Cognitive Neuroscience, 17, 507-517.
[16]
Gazzaley, A., Cooney, J. W., Rissman, J., & D'Esposito, M. (2005). Top-down suppression deficit underlies working memory impairment in normal aging. Nature Neuroscience, 8, 1298-1300.
[17]
Gazzaley, A., & Nobre, A. C. (2012). Top-down modulation: Bridging selective attention and working memory. Trends in Cognitive Sciences, 16, 129-135.
[18]
Gratton, G., Coles, M. G. H., & Donchin, E. (1983). A new method for off-line removal of ocular artifact. Electroencephalography and Clinical Neurophysiology, 55, 468-484.
[19]
Gross, J., Schmitz, F., Schnitzler, I., Kessler, K., Shapiro, K., Hommel, B., et al. (2004). Modulation of long-range neural synchrony reflects temporal limitations of visual attention in humans. Proceedings of the National Academy of Sciences, U.S.A., 101, 13050-13055.
[20]
Haegens, S., Osipova, D., Oostenveld, R., & Jensen, O. (2010). Somatosensory working memory performance in humans depends on both engagement and disengagement of regions in a distributed network. Human Brain Mapping, 31, 26-35.
[21]
Hanslmayr, S., Aslan, A., Staudigl, T., Klimesch, W., Herrmann, C. S., & Bäuml, K. H. (2007). Prestimulus oscillations predict visual perception performance between and within subjects. Neuroimage, 37, 1465-1473.
[22]
Hasher, L., & Zacks, R. T. (1988). Working memory, comprehension, and aging: A review and a new view. In G. H. Bower (Ed.), The psychology of learning and motivation (pp. 193-225). San Diego, CA: Academic Press.
[23]
Jensen, O., & Mazaheri, A. (2010). Shaping functional architecture by oscillatory alpha activity: Gating by inhibition. Frontiers in Human Neuroscience, 4, 186.
[24]
Kastner, S., & Ungerleider, L. G. (2000). Mechanisms of visual attention in the human cortex. Annual Review of Neuroscience, 23, 315-341.
[25]
Klimesch, W. (2011). Evoked alpha and early access to the knowledge system: The P1 inhibition timing hypothesis. Brain Research, 1408, 52-71.
[26]
Klimesch, W., Sauseng, P., & Hanslmayr, S. (2007). EEG alpha oscillations: The inhibition-timing hypothesis. Brain Research Reviews, 53, 63-88.
[27]
Knight, R. T., Staines, W. R., Swick, D., & Chao, L. L. (1999). Prefrontal cortex regulates inhibition and excitation in distributed neural networks. Acta Psychologica, 101, 159-178.
[28]
Kramer, A. F., Humphrey, D. G., Larish, J. F., Logan, G. D., & Strayer, D. L. (1994). Aging and inhibition: Beyond a unitary view of inhibitory processing in attention. Psychology and Aging, 9, 491-512.
[29]
Lachaux, J., Rodriguez, E., Martinerie, J., & Varela, F. J. (1999). Measuring phase synchrony in brain signals. Human Brain Mapping, 8, 194-208.
[30]
Lavie, N. (2005). Distracted and confused?: Selective attention under load. Trends in Cognitive Sciences, 9, 75-82.
[31]
Lavie, N., Hirst, A., De Fockert, J. W., & Viding, E. (2004). Load theory of selective attention and cognitive control. Journal of Experimental Psychology: General, 133, 339-354.
[32]
Li, S. C., & Sikström, S. (2002). Integrative neurocomputational perspectives on cognitive aging, neuromodulation, and representation. Neuroscience and Biobehavioral Reviews, 26, 795-808.
[33]
Mager, R., Bullinger, A. H., Brand, S., Schmidlin, M., Schärli, H., Müller-Spahn, F., et al. (2007). Age-related changes in cognitive conflict processing: An event-related potential study. Neurobiology of Aging, 28, 1925-1935.
[34]
Mangun, G. R., & Hillyard, S. A. (1991). Modulations of sensory-evoked brain potentials indicate changes in perceptual processing during visual-spatial priming. Journal of Experimental Psychology: Human Perception and Performance, 17, 1057-1074.
[35]
Meeuwissen, E. B., Takashima, A., Fernandez, G., & Jensen, O. (2011). Increase in posterior alpha activity during rehearsal predicts successful long-term memory formation of word sequences. Human Brain Mapping, 32, 2045-2053.
[36]
Miller, B. T., & D'Esposito, M. (2005). Searching for "the top" in top-down control. Neuron, 48, 535-538.
[37]
Nagel, I. E., Preuschhof, C., Li, S. C., Nyberg, L., Bäckman, L., Lindenberger, U., et al. (2009). Performance level modulates adult age differences in brain activation during spatial working memory. Proceedings of the National Academy of Sciences, U.S.A., 106, 22552-22557.
[38]
Noudoost, B., Chang, M. H., Steinmetz, N. A., & Moore, T. (2010). Top-down control of visual attention. Current Opinion in Neurobiology, 20, 183-190.
[39]
Oostenveld, R., Fries, P., Maris, E., & Schoffelen, J.-M. (2011). FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Computational Intelligence and Neuroscience, 2011:156869.
[40]
Park, D. C., Polk, T. A., Park, R., Minear, M., Savage, A., & Smith, M. R. (2004). Aging reduces neural specialization in ventral visual cortex. Proceedings of the National Academy of Sciences, U.S.A., 101, 13091-13095.
[41]
Park, D. C., & Reuter-Lorenz, P. (2009). The adaptive brain: Aging and neurocognitive scaffolding. Annual Review of Psychology, 60, 173-196.
[42]
Pinsk, M. A., Doniger, G. M., & Kastner, S. (2004). Push-pull mechanism of selective attention in human extrastriate cortex. Journal of Neurophysiology, 92, 622-629.
[43]
Posner, M. I., & Petersen, S. E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13, 25-42.
[44]
Raz, A., & Buhle, J. (2006). Typologies of attentional networks. Nature Reviews Neuroscience, 7, 367-379.
[45]
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.
[46]
Reuter-Lorenz, P. A., & Cappell, K. A. (2008). Neurocognitive aging and the compensation hypothesis. Current Directions in Psychological Science, 17, 177-182.
[47]
Sauseng, P., & Klimesch, W. (2008). What does phase information of oscillatory brain activity tell us about cognitive processes? Neuroscience and Biobehavioral Reviews, 32, 1001-1013.
[48]
Schmandt, B., Lindeboom, J., & van Harskamp, F. (1992). NLV Nederlandse Leestest voor Volwassenen Handleiding {Manual Dutch Adult Reading Test}. Lisse, The Netherlands: Swets & Zeitlinger.
[49]
Uterwijk, J. (2001). WAIS-III Nederlandstalige bewerking. Technische handleiding {Manual Dutch adaptationWAIS-III}. Lisse, The Netherlands: Swets & Zeitlinger.
[50]
Vogel, E. K., & Luck, S. J. (2000). The visual N1 component as an index of a discrimination process. Psychophysiology, 37, 190-203.
[51]
Von Stein, A., Chiang, C., & König, P. (2000). Top-down processing mediated by interareal synchronization. Proceedings of the National Academy of Sciences, U.S.A., 97, 14748-14753.
[52]
Wijers, A. A., Okita, T., Mulder, G., Mulder, L. J., Lorist, M. M., Poiesz, R., et al. (1987). Visual search and spatial attention: ERPs in focussed and divided attention conditions. Biological Psychology, 25, 33-60.
[53]
Wild-Wall, N., Falkenstein, M., & Hohnsbein, J. (2008). Flanker interference in young and older participants as reflected in event-related potentials. Brain Research, 1211, 72-84.
[54]
Wróbel, A. (2000). Beta activity: A carrier for visual attention. Acta Neurobiologiae Experimentalis, 60, 247-260.
[55]
Wróbel, A., Ghazaryan, A., Bekisz, M., Bogdan, W., & Kaminski, J. (2007). Two streams of attention-dependent ß activity in the striate recipient zone of cat's lateral posterior-pulvinar complex. The Journal of Neuroscience, 27, 2230-2240.
[56]
Zanto, T. P., & Gazzaley, A. (2009). Neural suppression of irrelevant information underlies optimal working memory performance. The Journal of Neuroscience, 29, 3059-3066.
[57]
Zanto, T. P., Rubens, M. T., Bollinger, J., & Gazzaley, A. (2010). Top-down modulation of visual feature processing: The role of the inferior frontal junction. Neuroimage, 53, 736-745.
[58]
Zigmond, A. S., & Snaith, R. P. (1983). The hospital anxiety and depression scale. Acta Psychiatrica Scandinavica, 67, 361-370.
Recommendations
Functional connectivity and coactivation of the nucleus accumbens: A combined functional connectivity and structure-based meta-analysis
This article investigates the functional connectivity patterns of the nucleus accumbens (NAcc) in 18 healthy participants using a resting state functional connectivity (rsFC) protocol. Also, a meta-analytic connectivity modeling (MACM) was used to ...
Increased Functional Connectivity After Acupuncture Treatment for Patients with Post-Stroke Depression
ICBEB 2018: Proceedings of the 2nd International Conference on Biomedical Engineering and BioinformaticsThis study is to investigate the therapeutic effect of acupuncture treatment (ACT) on PSD through resting state functional connectivity analysis. The participants include seven PSD patients who have completed ACT trial and seven PSD patients who have ...
Increased facilitatory connectivity from the pre-sma to the left dorsal premotor cortex during pseudoword repetition
Previous studies have demonstrated that the repetition of pseudowords engages a network of premotor areas for articulatory planning and articulation. However, it remains unclear how these premotor areas interact and drive one another during speech ...
Comments
Information & Contributors
Information
Published In
Publisher
MIT Press
Cambridge, MA, United States
Publication History
Published: 01 October 2012
Qualifiers
- Article
Contributors
Other Metrics
Bibliometrics & Citations
Bibliometrics
Article Metrics
- 0Total Citations
- 0Total Downloads
- Downloads (Last 12 months)0
- Downloads (Last 6 weeks)0
Reflects downloads up to 11 Aug 2024
Other Metrics
Citations
View Options
View options
Get Access
Login options
Check if you have access through your login credentials or your institution to get full access on this article.
Sign in