The compensatory role of the frontal cortex in mild cognitive impairment: Identifying the target for neuromodulation

Authors

  • Olga R. Dobrushina Research Center of Neurology, Moscow, Russia https://orcid.org/0000-0002-9493-4212
  • Zukhra Sh. Gadzhieva Research Center of Neurology, Moscow, Russia
  • Sofya N Morozova Research Center of Neurology, Moscow, Russia
  • Elena I Kremneva Research Center of Neurology, Moscow, Russia
  • Marina V Krotenkova Research Center of Neurology, Moscow, Russia
  • Larisa A. Dobrynina Research Center of Neurology, Moscow, Russia

DOI:

https://doi.org/10.15540/nr.6.1.3

Keywords:

mild cognitive impairment, executive functions, fMRI, functional connectivity

Abstract

Introduction: Development of individualized neuromodulation techniques for mild cognitive impairment (MCI) is a feasible practical goal.  Preliminary research exploring the brain-level compensatory reserves on the base of neuroimaging is necessary.  Methods: Twenty-one older adults, representing a continuum from healthy norm to MCI, underwent functional MRI while performing two executive tasks—a modified Stroop task and selective counting.  A functional activation and connectivity analysis were conducted with the inclusion of a BRIEF–MoCA covariate.  This variable represented the difference between the real-life performance measured by Behavior Rating Inventory of Executive Function (BRIEF) and the level of cognitive deficit measured by Montreal Cognitive Assessment (MoCA) Scale, an ability to compensate for impairment.  Results: Both tasks were associated with activation of areas within the frontoparietal control network, along with the supplementary motor area (SMA) and the pre-SMA, the lateral premotor cortex, and the cerebellum.  A widespread increase in the connectivity of the pre-SMA was observed during the tasks.  The BRIEF–MoCA value correlated, first, with connectivity of the left dorsolateral prefrontal cortex (LDLPFC) and, second, with enrollment of the occipital cortex during the counting task.  Conclusion: The developed neuroimaging technique allows identification of the functionally salient target within the LDLPFC in patients with MCI.

Author Biography

Olga R. Dobrushina, Research Center of Neurology, Moscow, Russia

Olga R. Dobrushina is a Research Fellow of the Third Neurological Department. She recieved her M.D. degree from M.V. Lomonosov Moscow State University in 2008 and Ph.D. degree from Gereral Reanimatology Institute in 2012. She is also employed in the International Insitute of Psychosomatic Health as Director-General and Neurologist. Her main fields of interest are neurorehabilitation, neurofeedback and functional MRI.

References

Ahdab, R., Ayache, S. S., Brugières, P., Goujon, C., & Lefaucheur, J.-P. (2010). Comparison of “standard” and “navigated” procedures of TMS coil positioning over motor, premotor and prefrontal targets in patients with chronic pain and depression. Neurophysiologie Clinique = Clinical Neurophysiology, 40(1), 27–36.

Anderkova, L., Eliasova, I., Marecek, R., Janousova, E., & Rektorova, I. (2015). Distinct pattern of gray matter atrophy in mild Alzheimer’s disease impacts on cognitive outcomes of noninvasive brain stimulation. Journal of Alzheimer’s Disease, 48(1), 251–260. http://dx.doi.org/10.3233/JAD-150067

Bae, J. B., Han, J. W., Kwak, K. P., Kim, B. J., Kim, S. G., Kim, J. L., … Kim, K. W. (2018). Impact of mild cognitive impairment on mortality and cause of death in the elderly. Journal of Alzheimer’s Disease, 64(2), 607–616. http://dx.doi.org/10.3233/JAD-171182

Bashir, S., Edwards, D., & Pascual-Leone, A. (2011). Neuronavigation increases the physiologic and behavioral effects of low-frequency rTMS of primary motor cortex in healthy subjects. Brain Topography, 24(1), 54–64. http://dx.doi.org/10.1007/s10548-010-0165-7

Bush, G., Luu, P., & Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences, 4(6), 215–222. http://dx.doi.org/10.1016/S1364-6613(00)01483-2

Cieslik, E. C., Zilles, K., Caspers, S., Roski, C., Kellermann, T. S., Jakobs, O., … Eickhoff, S. B. (2013). Is there “one” DLPFC in cognitive action control? Evidence for heterogeneity from co-activation-based parcellation. Cerebral Cortex, 23(11), 2677–2689. http://dx.doi.org/10.1093/cercor/bhs256

Clément, F., Gauthier, S., & Belleville, S. (2013). Executive functions in mild cognitive impairment: Emergence and breakdown of neural plasticity. Cortex, 49(5), 1268–1279. http://dx.doi.org/10.1016/j.cortex.2012.06.004

Dehaene, S., Piazza, M., Pinel, P., & Cohen, L. (2003). Three parietal circuits for number processing. Cognitive Neuropsychology, 20(3–6), 487–506. http://dx.doi.org/10.1080/02643290244000239

Delis, D. C., Kaplan, E., & Kramer, J. H. (2001). Delis-Kaplan Executive Function System (D-KEFS): Examiner’s manual. San Antonio, TX: The Psychological Corporation.

Drumond Marra, H. L., Myczkowski, M. L., Maia Memória, C., Arnaut, D., Leite Ribeiro, P., Sardinha Mansur, C. G., … Marcolin, M. A. (2015). Transcranial magnetic stimulation to address mild cognitive impairment in the elderly: A randomized controlled study. Behavioural Neurology, 2015, 287843. http://dx.doi.org/10.1155/2015/287843

Dubois, B., Slachevsky, A., Litvan, I., & Pillon, B. (2000). The FAB: A frontal assessment battery at bedside. Neurology, 55(11), 1621–1626. http://dx.doi.org/10.1212/WNL.55.11.1621

Fazekas, F., Chawluk, J. B., Alavi, A., Hurtig, H. I., & Zimmerman, R. A. (1987). MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. American Journal of Roentgenology, 149(2), 351–356. http://dx.doi.org/10.2214/ajr.149.2.351

Fitzgerald, P. B., Hoy, K., McQueen, S., Maller, J. J., Herring, S., Segrave, R., … Daskalakis, Z. J. (2009). A randomized trial of rTMS targeted with MRI based neuro-navigation in treatment-resistant depression. Neuropsychopharmacology, 34(5), 1255–1262. http://dx.doi.org/10.1038/npp.2008.233

Flinker, A., Korzeniewska, A., Shestyuk, A. Y., Franaszczuk, P. J., Dronkers, N. F., Knight, R. T., & Crone, N. E. (2015). Redefining the role of Broca’s area in speech. Proceedings of the National Academy of Sciences of the United States of America, 112(9), 2871–2875. http://dx.doi.org/10.1073/pnas.1414491112

Fox, M. D., Liu, H., & Pascual-Leone, A. (2013). Identification of reproducible individualized targets for treatment of depression with TMS based on intrinsic connectivity. NeuroImage, 66, 151–160. http://dx.doi.org/10.1016/j.neuroimage.2012.10.082

Gioia, G. A., Isquith, P. K., Guy, S. C., & Kenworthy, L. (2000). TEST REVIEW Behavior Rating Inventory of Executive Function. Child Neuropsychology, 6(3), 235–238. http://dx.doi.org/10.1076/chin.6.3.235.3152

Hsu, N. S., Jaeggi, S. M., & Novick, J. M. (2017). A common neural hub resolves syntactic and non-syntactic conflict through cooperation with task-specific networks. Brain and Language, 166, 63–77. http://dx.doi.org/10.1016/j.bandl.2016.12.006

Hugo, J., & Ganguli, M. (2014). Dementia and cognitive impairment: Epidemiology, diagnosis, and treatment. Clinics in Geriatric Medicine, 30(3), 421–442. http://dx.doi.org/10.1016/j.cger.2014.04.001

Kaufmann, L., Ischebeck, A., Weiss, E., Koppelstaetter, F., Siedentopf, C., Vogel, S. E., … Wood, G. (2008). An fMRI study of the numerical Stroop task in individuals with and without minimal cognitive impairment. Cortex, 44(9), 1248–1255. http://dx.doi.org/10.1016/j.cortex.2007.11.009

Lima, C. F., Krishnan, S., & Scott, S. K. (2016). Roles of supplementary motor areas in auditory processing and auditory imagery. Trends in Neurosciences, 39(8), 527–542. http://dx.doi.org/10.1016/j.tins.2016.06.003

Luber, B. M., Davis, S., Bernhardt, E., Neacsiu, A., Kwapil, L., Lisanby, S. H., & Strauman, T. J. (2017). Using neuroimaging to individualize TMS treatment for depression: Toward a new paradigm for imaging-guided intervention. NeuroImage, 148, 1–7. http://dx.doi.org/10.1016/j.neuroimage.2016.12.083

Luria, A. R. (1980). Higher cortical functions in man. Second edition, revised and expanded. New York, NY: Basic Books.

Marshall, G. A., Rentz, D. M., Frey, M. T., Locascio, J. J., Johnson, K. A., Sperling, R. A., & Alzheimer’s Disease Neuroimaging Initiative. (2011). Executive function and instrumental activities of daily living in mild cognitive impairment and Alzheimer’s disease. Alzheimer’s & Dementia: The Journal of the Alzheimer’s Association, 7(3), 300–308. http://dx.doi.org/10.1016/j.jalz.2010.04.005

Nasreddine, Z. S., Phillips, N. A., Bédirian, V., Charbonneau, S., Whitehead, V., Collin, I., … Chertkow, H. (2005). The Montreal Cognitive Assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53(4), 695–699. http://dx.doi.org/10.1111/j.1532-5415.2005.53221.x

Naumczyk, P., Sabisz, A., Witkowska, M., Graff, B., Jodzio, K., Gąsecki, D., … Narkiewicz, K. (2017). Compensatory functional reorganization may precede hypertension-related brain damage and cognitive decline: A functional magnetic resonance imaging study. Journal of Hypertension, 35(6), 1252–1262. http://dx.doi.org/10.1097/HJH.0000000000001293

Petersen, R. C., Lopez, O., Armstrong, M. J., Getchius, T. S. D., Ganguli, M., Gloss, D., … Rae-Grant, A. (2018). Practice guideline update summary: Mild cognitive impairment. Neurology, 90(3), 126–135. http://dx.doi.org/10.1212/WNL.0000000000004826

Rizzolatti, G., Cattaneo, L., Fabbri-Destro, M., & Rozzi, S. (2014). Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. Physiological Reviews, 94(2), 655–706. http://dx.doi.org/10.1152/physrev.00009.2013

Sakai, K., Hikosaka, O., Miyauchi, S., Sasaki, Y., Fujimaki, N., & Pütz, B. (1999). Presupplementary motor area activation during sequence learning reflects visuo-motor association. The Journal of Neuroscience, 19(10), RC1.

Solé-Padullés, C., Bartrés-Faz, D., Junqué, C., Clemente, I. C., Molinuevo, J. L., Bargalló, N., … Valls-Solé, J. (2006). Repetitive transcranial magnetic stimulation effects on brain function and cognition among elders with memory dysfunction. A randomized sham-controlled study. Cerebral Cortex, 16(10), 1487–1493. http://dx.doi.org/10.1093/cercor/bhj083

Stroop, J. R. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 18(6), 643–662. http://dx.doi.org/10.1037/h0054651

Wilson, B. A., Gracey, F., Evans, J. J., & Bateman, A. (2009). Neuropsychological rehabilitation: Theory, models, therapy and outcome. Cambridge, UK: Cambridge University Press.

Zago, L., Petit, L., Turbelin, M.-R., Andersson, F., Vigneau, M., & Tzourio-Mazoyer, N. (2008). How verbal and spatial manipulation networks contribute to calculation: An fMRI study. Neuropsychologia, 46(9), 2403–2414. http://dx.doi.org/10.1016/j.neuropsychologia.2008.03.001

Zigmond, A. S., & Snaith, R. P. (1983). The hospital anxiety and depression scale. Acta Psychiatrica Scandinavica, 67(6), 361–370. http://dx.doi.org/10.1111/j.1600-0447.1983.tb09716.x

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Published

2019-03-24

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Research Papers