Skip to main content
Log in

Power and distribution of evoked gamma oscillations in brain aging and cognitive performance

  • Original Article
  • Published:
GeroScience Aims and scope Submit manuscript

Abstract

Aims

Gamma oscillations (≈25–100 Hz) are believed to play an essential role in cognition, and aberrant gamma oscillations occur in brain aging and neurodegeneration. This study examined age-related changes in visually evoked gamma oscillations at two different time points 5 years apart and tested the hypothesis that the power of gamma oscillations correlated to cognitive skills.

Methods

The cohort consists of elderly males belonging to the Metropolit 1953 Danish Male Birth Cohort (first visit, N=124; second visit, N=88) over a 5-year period from 63 to 68 years of age. Cognitive functions were assessed using a neuropsychological test battery measuring global cognition, intelligence, memory, and processing speed. The power of steady-state visual evoked potentials (SSVEP) was measured at 8 Hz (alpha) and 36 Hz (gamma) frequencies using EEG scalp electrodes.

Results

Over the 5-year period cognitive performance remained relatively stable while the power of visually evoked gamma oscillations shifted from posterior to anterior brain regions with increasing age. A higher-than-average cognitive score was correlated with higher gamma power in parieto-occipital areas and lower in frontocentral areas, i.e., preserved distribution of the evoked activity.

Conclusions

Our data reveal that the distribution of visually evoked gamma activity becomes distributed with age. Preserved posterior-occipital gamma power in participants with a high level of cognitive performance is consistent with a close association between the ability to produce gamma oscillations and cognition. The data may contribute to our understanding of the mechanisms that link evoked gamma activity and cognition in the aging brain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Rossini PM, Rossi S, Babiloni C, Polich J. Clinical neurophysiology of aging brain: from normal aging to neurodegeneration. Prog Neurobiol. 2007;83(6):375–400.

    Article  CAS  PubMed  Google Scholar 

  2. Ishii R, Canuet L, Aoki Y, Hata M, Iwase M, Ikeda S, Nishida K, Ikeda M. Healthy and pathological brain aging: from the perspective of oscillations, functional connectivity, and signal complexity. Neuropsychobiology. 2018;75(4):151–61.

    Article  Google Scholar 

  3. Perinelli A, Assecondi S, Tagliabue CF, Mazza V. Power shift and connectivity changes in healthy aging during resting-state EEG. NeuroImage. 2022;256:119247.

    Article  PubMed  Google Scholar 

  4. Murty DV, Manikandan K, Kumar WS, Ramesh RG, Purokayastha S, Javali M, Rao NP, Ray S. Gamma oscillations weaken with age in healthy elderly in human EEG. NeuroImage. 2020;215:116826.

    Article  PubMed  Google Scholar 

  5. Murty DV, Manikandan K, Kumar WS, Ramesh RG, Purokayastha S, Nagendra B, Abhishek ML, Balakrishnan A, Javali M, Rao NP, Ray S. Stimulus-induced gamma rhythms are weaker in human elderly with mild cognitive impairment and alzheimer’s disease. eLife. 2021;10:1–22.

    Article  CAS  Google Scholar 

  6. Herrmann CS, Struber D, Helfrich RF, Engel AK. EEG oscillations: from correlation to causal- ity. Int J Psychophysiol. 2016;103:12–21.

    Article  PubMed  Google Scholar 

  7. Klimesch W. Alpha-band oscillations, attention, and controlled access to stored information. Trends Cogn Sci. 2012;16(12):606–17.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Clayton FJ, Sears C, Davis A, Hulme C. Verbal task demands are key in explaining the relationship between paired-associate learning and reading ability. J Exp Child Psychol. 2018;171:46–54.

    Article  PubMed  Google Scholar 

  9. Gutteling TP, Sillekens L, Lavie N, Jensen O. Alpha oscillations reflect suppression of distractors with increased perceptual load. Prog Neurobiol. 2022;214:102285.

    Article  PubMed  Google Scholar 

  10. Herrmann CS, Munk MH, Engel AK. Cognitive functions of gamma-band activity: Memory match and utilization. Trends Cogn Sci. 2004;8(8):347–55.

    Article  PubMed  Google Scholar 

  11. Jensen O, Kaiser J, Lachaux JP. Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci. 2007;30(7):317–24.

    Article  CAS  PubMed  Google Scholar 

  12. Muller-Putz GR, Scherer R, Brauneis C, Pfurtscheller G. Steady-state visual evoked potential (SSVEP)-based communication: impact of harmonic frequency components. J Neural Eng. 2005;2(4):123–30.

    Article  PubMed  Google Scholar 

  13. Sharma K, Kar S. Extracting multiple commands from a single SSVEP flicker using eye accommodation. Biocybernetics Biomed Eng. 2019;39(3):914–22.

    Article  Google Scholar 

  14. Horwitz A, Thomsen MD, Wiegand I, Horwitz H, Klemp M, Nikolic M, Rask L, Lauritzen M, Benedek K. Visual steady state in relation to age and cognitive function. PLoS One. 2017;12(2):1–23.

    Article  Google Scholar 

  15. Vialatte FB, Maurice M, Dauwels J, Cichocki A. Steady-state visually evoked potentials: Focus on essential paradigms and future perspectives. Prog Neurobiol. 2010;90(4):418–38.

    Article  PubMed  Google Scholar 

  16. Silberstein RB, Nunez PL, Pipingas A, Harris P, Danieli F. Steady state visually evoked potential (SSVEP) topography in a graded working memory task. Int J Psychophysiol. 2001;42(2):219–32.

    Article  CAS  PubMed  Google Scholar 

  17. Kabdebon C, Flo A, de Heering A, Aslin R. The power of rhythms: how steady-state evoked responses reveal early neurocognitive development. NeuroImage. 2022;254:119150.

  18. Calderone DJ, Lakatos P, Butler PD, Castellanos FX. Entrainment of neural oscillations as a modifiable substrate of attention. Trends Cogn Sci. 2014;18(6):300–9.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Horwitz A, Klemp M, Horwitz H, Thomsen MD, Rostrup E, Mortensen EL, Osler M, Lauritzen M, Benedek K. Brain responses to passive sensory stimulation correlate with intelligence. Front Aging Neurosci. 2019;10:1–17.

    Google Scholar 

  20. Richard N, Nikolic M, Mortensen EL, Osler M, Lauritzen M, Benedek K. Steady-state visual evoked potential temporal dynamics reveal correlates of cognitive decline. Clin Neurophysiol. 2020;131(4):836–46.

    Article  PubMed  Google Scholar 

  21. Osler M, Lund R, Kriegbaum M, Christensen U, Andersen AMN. Cohort profile: the Metropolit 1953 Danish male birth cohort. Int J Epidemiol. 2006;35(3):541–5.

    Article  PubMed  Google Scholar 

  22. Zarnani K, Nichols TE, Alfaro-Almagro F, Fagerlund B, Lauritzen M, Rostrup E, Smith SM. Discovering markers of healthy aging: a prospective study in a Danish male birth cohort. Aging. 2019;11(16):5943–74.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Horwitz A, Mortensen EL, Osler M, Fagerlund B, Lauritzen M, Benedek K. Passive double sensory evoked coherence correlates with long-term memory capacity. Front Hum Neurosci. 2017;11:1–21.

    Article  Google Scholar 

  24. Vestergaard MB, Lindberg U, Knudsen MH, Urdanibia-Centelles O, Bakhtiari A, Mortensen EL, Osler M, Fagerlund B, Benedek K, Lauritzen M, Larsson HBW. Subclinical cognitive deficits are associated with reduced cerebrovascular response to visual stimulation in mid-sixties men. GeroScience. 2022;0123456789.

  25. Keil A, Muller MM, Ray WJ, Gruber T, Elbert T. Human gamma band activity and perception of a gestalt. J Neurosci. 1999;19(16):7152–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Schadow J, Lenz D, Thaerig S, Busch NA, Frund I, Rieger JW, Herrmann CS. Stimulus intensity affects early sensory processing: visual contrast modulates evoked gamma-band activity in human EEG. Int J Psychophysiol. 2007;66(1):28–36.

    Article  PubMed  Google Scholar 

  27. Joon Kim Y, Grabowecky M, Paller KA, Muthu K, Suzuki S. Attention induces synchronization based response gain in steady-state visual evoked potentials. Nat Neurosci. 2007;10(1):117–25.

    Article  Google Scholar 

  28. Delorme A, Makeig S. EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods. 2004;134(1):9–21.

    Article  PubMed  Google Scholar 

  29. Pion-Tonachini L, Kreutz-Delgado K, Makeig S. ICLabel: An automated electroencephalographic independent component classifier, dataset, and website. NeuroImage. 2019;198(April):181–97.

    Article  PubMed  Google Scholar 

  30. Perrin F, Pernier J, Bertrand O. Spherical splines for scalp potential and current density mapping 10.1016/0013-4694(89)90180-6: electroencephalography and clinical neurophysiology — ScienceDirect.com. Electroencephajogr Clin Neurophysiol. 1989;72(2):184–7.

    Article  CAS  Google Scholar 

  31. Welch PD. The use of fast Fourier transform for the estimation of power spectra: a method based on time averaging over short, modified periodograms. IEEE Trans Audio Electroacoust. 1967;15(2):70–3.

    Article  Google Scholar 

  32. Gaetz W, Roberts TP, Singh KD, Muthukumaraswamy SD. Functional and structural correlates of the aging brain: relating visual cortex (V1) gamma band responses to age-related structural change. Hum Brain Mapp. 2012;33(9):2035–46.

    Article  PubMed  Google Scholar 

  33. Fjell AM, Westlye LT, Grydeland H, Amlien I, Espeseth T, Reinvang I, Raz N, Dale AM, Walhovd KB. Accelerating cortical thinning: unique to dementia or universal in aging? Cereb Cortex. 2014;24(4):919–34.

    Article  PubMed  Google Scholar 

  34. Hedden T, Gabrieli JD. Insights into the ageing mind: a view from cognitive neuroscience. Nat Rev Neurosci. 2004;5(2):87–96.

    Article  CAS  PubMed  Google Scholar 

  35. Davis SW, Dennis NA, Daselaar SM, Fleck MS, Cabeza R. Que PASA? The posterior-anterior shift in aging. Cereb Cortex. 2008;18(5):1201–9.

    Article  PubMed  Google Scholar 

  36. Sullivan EV, Adalsteinsson E, Hedehus M, Ju C, Moseley M, Lim KO, Pfefferbaum A. Equivalent disruption of regional white matter microstructure in ageing healthy men and women. NeuroReport. 2001;12(1):99–104.

    Article  CAS  PubMed  Google Scholar 

  37. Peters A. The effects of normal aging on myelin and nerve fibers: a review. J Neurocytol. 2002;31(8-9):581–93.

    Article  PubMed  Google Scholar 

  38. Hong SL, Rebec GV. A new perspective on behavioral inconsistency and neural noise in aging: compensatory speeding of neural communication. Front Aging Neurosci. 2012;4:1–6.

  39. Fries P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci. 2005;9(10):474–80.

    Article  PubMed  Google Scholar 

  40. Lehmann K, Steinecke A, Bolz J. GABA through the ages: regulation of cortical function and plasticity by inhibitory interneurons. Neural Plasticity. 2012;2012.

  41. Gonzalez-Burgos G, Lewis DA. GABA neurons and the mechanisms of network oscillations: implications for understanding cortical dysfunction in schizophrenia. Schizophr Bull. 2008;34(5):944–61.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Prevot T, Sibille E. Altered GABA-mediated information processing and cognitive dysfunctions in´ depression and other brain disorders. Mol Psychiatry. 2021;26(1):151–67.

    Article  CAS  PubMed  Google Scholar 

  43. Bishop NA, Lu T, Yankner BA. Neural mechanisms of ageing and cognitive decline. Nature. 2010;464(7288):529–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Mably AJ, Colgin LL. Gamma oscillations in cognitive disorders. Curr Opin Neurobiol. 2018;52:182–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Han C, Shapley R, Xing D. Gamma rhythms in the visual cortex: functions and mechanisms. Cogn Neurodyn. 2022;16(4):745–56.

    Article  PubMed  Google Scholar 

  46. Traikapi A, Konstantinou N. Gamma oscillations in Alzheimer’s disease and their potential therapeutic role. Front Syst Neurosci. 2021;15.

  47. Lundqvist M, Rose J, Herman P, Brincat SLL, Buschman TJJ, Miller EKK. Gamma and beta bursts underlie working memory. Neuron. 2016;90(1):152–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Yamamoto J, Suh J, Takeuchi D, Tonegawa S. Successful execution of working memory linked to synchronized high-frequency gamma oscillations. Cell. 2014;157(4):845–57.

    Article  CAS  PubMed  Google Scholar 

  49. Fries P. Rhythms for cognition: communication through coherence. Neuron. 2015;88(1):220–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Ferretti A, Rogers-Healion K, Fotros A. The therapeutic potential of restoring gamma oscillations in Alzheimer’s disease. Adv Psychiatry Behav Health. 2022;2(1):47–55.

    Article  Google Scholar 

  51. Puttaert D, Coquelet N, Wens V, Peigneux P, Fery P, Rovai A, Trotta N, Sadeghi N, Coolen T, Bier JC, Goldman S, De Tiege X. Alterations in resting-state network dynamics along the Alzheimer’s` disease continuum. Sci Rep. 2020;10(1):1–13.

    Article  Google Scholar 

  52. Adaikkan C, Tsai LH. Gamma entrainment: impact on neurocircuits, glia, and therapeutic opportunities. Trends Neurosci. 2020;43(1):24–41.

    Article  CAS  PubMed  Google Scholar 

  53. Chan D, Suk H-J, Jackson BL, Milman NP, Stark D, Klerman EB, Kitchener E, Fernandez Avalos VS, Banerjee A, Beach SD, Blanchard J, Stearns C, Boes A, Uitermarkt B, Gander P, Howard M III, Sternberg EJ, Nieto-Castanon A, Anteraper S, et al. Gamma frequency sensory stimulation in probable mild Alzheimer’s dementia patients: results of a preliminary clinical trial. SSRN Electron J. 2021.

  54. Clements-Cortes A, Ahonen H, Evans M, Freedman M, Bartel L. Short-term effects of rhythmic sensory stimulation in Alzheimer’s disease: an exploratory pilot study. J Alzheimers Dis. 2016;52(2):651–60.

    Article  PubMed  Google Scholar 

  55. He Q, Colon-Motas KM, Pybus AF, Piendel L, Seppa JK, Walker ML, Manzanares CM, Qiu D, Miocinovic S, Wood LB, Levey AI, Lah JJ, Singer AC. A feasibility trial of gamma sensory flicker for patients with prodromal Alzheimer’s disease. Alzheimer’s Dementia. 2021;7(1):1–11.

    CAS  Google Scholar 

  56. Cabeza R, Albert M, Belleville S, Craik FI, Duarte A, Grady CL, Lindenberger U, Nyberg L, Park DC, Reuter-Lorenz PA, Rugg MD, Steffener J, Rajah MN. Maintenance, reserve and compensation: the cognitive neuroscience of healthy ageing. Nat Rev Neurosci. 2018;19(11):701–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Koen JD, Rugg MD. Neural dedifferentiation in the aging brain. Trends Cogn Sci. 2019;23(7):547–59.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Schaworonkow N, Nikulin VV. Is sensor space analysis good enough? Spatial patterns as a tool for assessing spatial mixing of EEG/MEG rhythms. NeuroImage. 2022;253:119093.

    Article  PubMed  Google Scholar 

  59. Zhang Y, Xu P, Huang Y, Cheng K, Yao D. SSVEP response is related to functional brain network topology entrained by the flickering stimulus. PLoS One. 2013;8(9).

Download references

Acknowledgements

We want to thank Sine Kongsbak Arvedsen and Natalia Christina Brandstrup for their work with coordinating the project and the extensive data collection. We also thank Keng Wah Niels Pang and Miki Nikolic for all technical assistance and their valuable input on processing of the EEG data.

Funding

The study was supported by a Nordea Foundation Grant to the Center for Healthy Ageing at the University of Copenhagen. The Copenhagen Ageing and Midlife Biobank is supported by grants from the Velux Foundation (VELUX26145 and 31539).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aftab Bakhtiari.

Ethics declarations

Ethical approval and consent to participate

The study was approved by the Capital Region of Denmark’s Committee on Health Research Ethics (H-1–2014032). All participants provided written consent regarding their participation and publication of the current data.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bakhtiari, A., Petersen, J., Urdanibia-Centelles, O. et al. Power and distribution of evoked gamma oscillations in brain aging and cognitive performance. GeroScience 45, 1523–1538 (2023). https://doi.org/10.1007/s11357-023-00749-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11357-023-00749-x

Keywords

Navigation