Skip to main content

Advertisement

SpringerLink
Log in

Reduced spontaneous low frequency oscillations as measured with functional near-infrared spectroscopy in mild cognitive impairment

  • ORIGINAL RESEARCH
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Spontaneous low frequency oscillations (LFO) in functional imaging data have gained increased interest in the study of cognitive decline. Persons diagnosed with mild cognitive impairment (MCI) and Alzheimer’s disease (AD) display alterations in their amount of LFO in various brain regions. This is commonly interpreted as disruptions in the autoregulation of the cerebral microvascular system. In the present study LFO (0,07–0,11 Hz) were measured with 52-channel near-infrared spectroscopy (NIRS) in 61 healthy elderly persons (70–76 years), 54 MCI subjects (70–76 years) and 25 healthy young controls (21–48 years) during rest over the frontal and the parietal cortex. Both MCI and healthy elderly controls showed less LFO in the frontal cortex as compared to young subjects. For the parietal cortex a decrease in LFO could be observed for the MCI group in comparison to healthy elderly subjects. Correlations of more LFO with worse performance in neuropsychological tests point to compensatory processes. LFO measured with NIRS might be especially suited for longitudinal studies aiming at predicting cognitive decline.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Beck, A. T., Steer, R. A., & Brown, G. K. (1996). Beck depression inventory-II. San Antonio.

  • Biswal, B., Yetkin, F. Z., Haughton, V. M., & Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic Resonance in Medicine, 34(4), 537–541.

    Article  CAS  Google Scholar 

  • Caselli, R. J., Chen, K., Lee, W., Alexander, G. E., & Reiman, E. M. (2008). Correlating cerebral hypometabolism with future memory decline in subsequent converters to amnestic pre-mild cognitive impairment. Archives of Neurology, 65(9), 1231–1236. https://doi.org/10.1001/archneurol.2008.1.

    Article  PubMed  Google Scholar 

  • DeCarli, C. (2003). Mild cognitive impairment: prevalence, prognosis, aetiology, and treatment. Lancet Neurology, 2(1), 15–21.

    Article  Google Scholar 

  • Desai, A. K., & Grossberg, G. T. (2005). Diagnosis and treatment of Alzheimer’s disease. Neurology, 64(12 Suppl 3), S34–S39.

    Article  CAS  Google Scholar 

  • Elwell, C. E., Owen-Reece, H., Wyatt, J. S., Cope, M., Reynolds, E. O., & Delpy, D. T. (1996). Influence of respiration and changes in expiratory pressure on cerebral haemoglobin concentration measured by near infrared spectroscopy. Journal of Cerebral Blood Flow Metabolism, 16(2), 353–357. https://doi.org/10.1097/00004647-199603000-00022.

    Article  CAS  PubMed  Google Scholar 

  • Erzigkeit, H., Lehfeld, H., Pena-Casanova, J., Bieber, F., Yekrangi-Hartmann, C., Rupp, M.,… Hindmarch, I. (2001). The Bayer-Activities of Daily Living Scale (B-ADL): results from a validation study in three European countries. Dementia and Geriatric Cognitive Disorders, 12(5), 348–358. https://doi.org/10.1159/000051280.

    Article  CAS  PubMed  Google Scholar 

  • Fallgatter, A. J., Ehlis, A. C., Wagener, A., Michel, T., & Herrmann, M. J. (2004). Near-infrared spectroscopy in psychiatry. Nervenarzt, 75(9), 911–916.

    Article  CAS  Google Scholar 

  • Farkas, E., & Luiten, P. G. (2001). Cerebral microvascular pathology in aging and Alzheimer’s disease. Progress in Neurobiology, 64(6), 575–611.

    Article  CAS  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(3), 189–198.

    Article  CAS  Google Scholar 

  • Frisoni, G. B., Lorenzi, M., Caroli, A., Kemppainen, N., Nagren, K., & Rinne, J. O. (2009). In vivo mapping of amyloid toxicity in Alzheimer disease. Neurology, 72(17), 1504–1511. https://doi.org/10.1212/WNL.0b013e3181a2e896.

    Article  CAS  PubMed  Google Scholar 

  • Gauggel, S., & Birkner, B. (1999). Validity and reliability of a German version of the Geriatric Depression Scale (GDS). Zeitschrift Fur Klinische Psychologie-Forschung Und Praxis, 28(1), 18–27. https://doi.org/10.1026//0084-5345.28.1.18.

    Article  Google Scholar 

  • Hachinski, V. C., Iliff, L. D., Zilhka, E., et al. (1975). Cerebral blood flow in dementia. Archives of Neurology, 32(9), 632–637. https://doi.org/10.1001/archneur.1975.00490510088009.

    Article  CAS  PubMed  Google Scholar 

  • Han, B. H., Zhou, M. L., Abousaleh, F., Brendza, R. P., Dietrich, H. H., Koenigsknecht-Talboo, J.,… Zipfel, G. J. (2008). Cerebrovascular dysfunction in amyloid precursor protein transgenic mice: contribution of soluble and insoluble amyloid-beta peptide, partial restoration via gamma-secretase inhibition. Journal of Neuroscience, 28(50), 13542–13550. https://doi.org/10.1523/jneurosci.4686-08.2008.

    Article  CAS  PubMed  Google Scholar 

  • Hautzinger, M., Keller, F., & Kühner, C. (2006). Beck Depressions-Inventar (BDI-II). Revision. Frankfurt am Main: Harcourt Test Services.

    Google Scholar 

  • Helmstaedter, C., Lendt, M., & Lux, S. (2001). Verbaler Lern- und Merkfähigkeitstest: VLMT. Göttingen: Beltz Test GmbH.

    Google Scholar 

  • Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6(2), 65–70.

    Google Scholar 

  • Jasper, H. (1958). Report of committee on methods of clinical exam in EEG. Electroencephalography and Clinical Neurophysiology Supply, 10, 370–375.

    Article  Google Scholar 

  • Jicha, G. A., Parisi, J. E., Dickson, D. W., Johnson, K., Cha, R., Ivnik, R. J.,… Petersen, R. C (2006). Neuropathologic outcome of mild cognitive impairment following progression to clinical dementia. Archives of Neurology, 63(5), 674–681. https://doi.org/10.1001/archneur.63.5.674.

  • Julien, C. (2006). The enigma of Mayer waves: facts and models. Cardiovascular Research, 70(1), 12–21. https://doi.org/10.1016/j.cardiores.2005.11.008.

    Article  CAS  PubMed  Google Scholar 

  • Kalbe, E., Kessler, J., Calabrese, P., Smith, R., Passmore, A. P., Brand, M., & Bullock, R. (2004). DemTect: a new, sensitive cognitive screening test to support the diagnosis of mild cognitive impairment and early dementia. International Journal of Geriatric Psychiatry, 19(2), 136–143. https://doi.org/10.1002/gps.1042.

    Article  CAS  PubMed  Google Scholar 

  • Muller, L. D., Guhn, A., Zeller, J. B., Biehl, S. C., Dresler, T., Hahn, T.,.. . Herrmann, M. J. (2014). Neural correlates of a standardized version of the trail making test in young and elderly adults: a functional near-infrared spectroscopy study. Neuropsychologia, 56, 271–279. https://doi.org/10.1016/j.neuropsychologia.2014.01.019.

    Article  PubMed  Google Scholar 

  • Obrig, H., Neufang, M., Wenzel, R., Kohl, M., Steinbrink, J., Einhaupl, K., & Villringer, A. (2000). Spontaneous low frequency oscillations of cerebral hemodynamics and metabolism in human adults. Neuroimage, 12(6), 623–639. https://doi.org/10.1006/nimg.2000.0657.

    Article  CAS  PubMed  Google Scholar 

  • Obrig, H., & Villringer, A. (2003). Beyond the visible–imaging the human brain with light. Journal of Cerebral Blood Flow Metabolism, 23(1), 1–18.

    Article  Google Scholar 

  • Okamoto, M., Dan, H., Sakamoto, K., Takeo, K., Shimizu, K., Kohno, S.,.. . Dan, I. (2004). Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping. Neuroimage, 21(1), 99–111.

    Article  Google Scholar 

  • Petersen, R. C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256(3), 183–194. https://doi.org/10.1111/j.1365-2796.2004.01388.x.

    Article  CAS  PubMed  Google Scholar 

  • Petersen, R. C., Smith, G. E., Waring, S. C., Ivnik, R. J., Tangalos, E. G., & Kokmen, E. (1999). Mild cognitive impairment: clinical characterization and outcome. Archives of Neurology, 56(3), 303–308.

    Article  CAS  Google Scholar 

  • Polak, T., Herrmann, M. J., Muller, L. D., Zeller, J. B. M., Katzorke, A., Fischer, M.,.… Deckert, J. (2017). Near-infrared spectroscopy (NIRS) and vagus somatosensory evoked potentials (VSEP) in the early diagnosis of Alzheimer’s disease: rationale, design, methods, and first baseline data of the Vogel study. Journal of Neural Transmission (Vienna). https://doi.org/10.1007/s00702-017-1781-0.

    Article  Google Scholar 

  • Portet, F., Ousset, P. J., Visser, P. J., Frisoni, G. B., Nobili, F., Scheltens, P.,.… Disease, M. C. I. W. G. o. t. E. C. o. A. s. (2006). Mild cognitive impairment (MCI) in medical practice: a critical review of the concept and new diagnostic procedure. report of the MCI Working Group of the European Consortium on Alzheimer’s Disease. Journal of Neurology Neurosurgery and Psychiatry, 77(6), 714–718. https://doi.org/10.1136/jnnp.2005.085332.

    Article  CAS  Google Scholar 

  • Rosen, W. G., Terry, R. D., Fuld, P. A., Katzman, R., & Peck, A. (1980). Pathological verification of ischemic score in differentiation of dementias. Annals of Neurology, 7(5), 486–488. https://doi.org/10.1002/ana.410070516.

    Article  CAS  PubMed  Google Scholar 

  • Schroeter, M. L., Bucheler, M. M., Preul, C., Scheid, R., Schmiedel, O., Guthke, T., & von Cramon, D. Y. (2005). Spontaneous slow hemodynamic oscillations are impaired in cerebral microangiopathy. Journal of Cerebral Blood Flow & Metabolism, 25(12), 1675–1684. https://doi.org/10.1038/sj.jcbfm.9600159.

    Article  Google Scholar 

  • Schroeter, M. L., Schmiedel, O., & von Cramon, D. Y. (2004). Spontaneous low-frequency oscillations decline in the aging brain. Journal of Cerebral Blood Flow & Metabolism, 24(10), 1183–1191. https://doi.org/10.1097/01.wcb.0000135231.90164.40.

    Article  Google Scholar 

  • Sorg, C., Riedl, V., Muhlau, M., Calhoun, V. D., Eichele, T., Laer, L.,.… Wohlschlager, A. M. (2007). Selective changes of resting-state networks in individuals at risk for Alzheimer’s disease. Proceeding of the National Academy of Sciences of the United States of America, 104(47), 18760–18765. https://doi.org/10.1073/pnas.0708803104.

    Article  Google Scholar 

  • Tong, Y., & Frederick, B. D. (2010). Time lag dependent multimodal processing of concurrent fMRI and near-infrared spectroscopy (NIRS) data suggests a global circulatory origin for low-frequency oscillation signals in human brain. Neuroimage, 53(2), 553–564. https://doi.org/10.1016/j.neuroimage.2010.06.049.

    Article  PubMed  PubMed Central  Google Scholar 

  • van Beek, A. H., Lagro, J., Olde-Rikkert, M. G., Zhang, R., & Claassen, J. A. (2012). Oscillations in cerebral blood flow and cortical oxygenation in Alzheimer’s disease. Neurobiology of Aging, 33(2), 428 e421–431. https://doi.org/10.1016/j.neurobiolaging.2010.11.016.

  • Vermeij, A., Meel-van den Abeelen, A. S., Kessels, R. P., van Beek, A. H., & Claassen, J. A. (2014). Very-low-frequency oscillations of cerebral hemodynamics and blood pressure are affected by aging and cognitive load. Neuroimage, 85 Pt, 1, 608–615. https://doi.org/10.1016/j.neuroimage.2013.04.107.

    Article  Google Scholar 

  • Winblad, B., Amouyel, P., Andrieu, S., Ballard, C., Brayne, C., Brodaty, H.,.… Zetterberg, H. (2016). Defeating Alzheimer’s disease and other dementias: a priority for European science and society. Lancet Neurology, 15(5), 455–532. https://doi.org/10.1016/s1474-4422(16)00062-4.

    Article  PubMed  Google Scholar 

  • Wu, Z., Guo, H., Chow, N., Sallstrom, J., Bell, R. D., Deane, R.,… Zlokovic, B. V. (2005). Role of the MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer disease. Nature Medicine, 11(9), 959–965. https://doi.org/10.1038/nm1287.

    Article  CAS  PubMed  Google Scholar 

  • Yesavage, J. A., Brink, T. L., Rose, T. L., Lum, O., Huang, V., Adey, M., & Leirer, V. O. (1982). Development and validation of a geriatric depression screening scale: a preliminary report. Journal of Psychiatric Research, 17(1), 37–49.

    Article  Google Scholar 

  • Zeller, J. B., Herrmann, M. J., Ehlis, A. C., Polak, T., & Fallgatter, A. J. (2010). Altered parietal brain oxygenation in Alzheimer’s disease as assessed with near-infrared spectroscopy. American Journal of Geriatric Psychiatry, 18(5), 433–441. https://doi.org/10.1097/JGP.0b013e3181c65821.

    Article  PubMed  Google Scholar 

  • Zhang, R., Zuckerman, J. H., Giller, C. A., & Levine, B. D. (1998). Transfer function analysis of dynamic cerebral autoregulation in humans. American Journal of Physiology, 274(1 Pt 2), H233–H241.

    CAS  PubMed  Google Scholar 

  • Zhao, Z., Fan, F. M., Lu, J., Li, H. J., Jia, L. F., Han, Y., & Li, K. C. (2015). Changes of gray matter volume and amplitude of low-frequency oscillations in amnestic MCI: an integrative multi-modal MRI study. Acta Radiologica, 56(5), 614–621. https://doi.org/10.1177/0284185114533329.

    Article  PubMed  Google Scholar 

  • Zhao, Z., Lu, J., Jia, X., Chao, W., Han, Y., Jia, J., & Li, K. (2014). Selective changes of resting-state brain oscillations in aMCI: an fMRI study using ALFF. Biomed Research International, 2014, 920902. https://doi.org/10.1155/2014/920902.

Download references

Acknowledgements

We gratefully acknowledge the assistance of Mrs. Stefanie Karl, Mrs. Nina Weißenberger and Mrs. Inge Gröbner.

Author information

Authors and Affiliations

  1. Department of Psychiatry, Psychosomatics and Psychotherapy, Center of Mental Health, University Hospital Würzburg, Margarete-Höppel-Platz 1, 97080, Würzburg, Germany

    Julia B. M. Zeller, Andrea Katzorke, Laura D. Müller, Judith Breunig, Jürgen Deckert, Bodo Warrings, Martin Lauer, Thomas Polak & Martin J. Herrmann

  2. Department of Psychiatry and Psychotherapy, University Hospital Tübingen, Calwerstraße 14, 72076, Tübingen, Germany

    Florian B. Haeussinger

Authors
  1. Julia B. M. Zeller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea Katzorke
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura D. Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Judith Breunig
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Florian B. Haeussinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jürgen Deckert
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bodo Warrings
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Martin Lauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Thomas Polak
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Martin J. Herrmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin J. Herrmann.

Ethics declarations

Disclosure of potential conflicts of interest

This study was funded by a research grant of the “Vogelstiftung Dr. Eckernkamp”, Würzburg, Germany. The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

This work is part of the dissertation of Judith Breunig.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zeller, J.B.M., Katzorke, A., Müller, L.D. et al. Reduced spontaneous low frequency oscillations as measured with functional near-infrared spectroscopy in mild cognitive impairment. Brain Imaging and Behavior 13, 283–292 (2019). https://doi.org/10.1007/s11682-018-9827-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-018-9827-y

Keywords

Search

Navigation