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Neuroscience Bulletin

, Volume 34, Issue 6, pp 963–971 | Cite as

A Longitudinal Functional Magnetic Resonance Imaging Study of Working Memory in Patients Following a Transient Ischemic Attack: A Preliminary Study

  • Wei Su
  • Jian Guo
  • Yun Zhang
  • Jie Zhou
  • Ning Chen
  • Muke Zhou
  • Rong Li
  • Huafu Chen
  • Li HeEmail author
Original Article
  • 109 Downloads

Abstract

In this study, we used functional magnetic resonance imaging (fMRI) to investigate longitudinal changes in brain activation during a verbal working memory (VWM) task performed by patients who had experienced a transient ischemic attack (TIA). Twenty-five first-ever TIA patients without visible lesions in conventional MRI and 25 healthy volunteers were enrolled. VWM task-related fMRI was conducted 1 week and 3 months post-TIA. The brain activity evoked by the task and changes over time were assessed. We found that, compared with controls, patients exhibited an increased activation in the bilateral inferior frontal gyrus (IFG), right dorsolateral prefrontal cortex (DLPFC), insula, inferior parietal lobe (IPL), and cerebellum during the task performed 1 week post-TIA. But only the right IFG still exhibited an increased activation at 3 months post-TIA. A direct comparison of fMRI data between 1 week and 3 months post-TIA showed greater activation in the bilateral middle temporal gyrus, right DLPFC, IPL, cerebellum, and left IFG in patients at 1 week post-TIA. We conclude that brain activity patterns induced by a VWM task remain dynamic for a period of time after a TIA, despite the cessation of clinical symptoms. Normalization of the VWM activation pattern may be progressively achieved after transient episodes of ischemia in TIA patients.

Keywords

Functional magnetic resonance imaging Recovery Transient ischemic attack Verbal working memory 

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (81300943 and 81472162) and the Postdoctoral Science Special Foundation of China (2014T70867).

Compliance with Ethical Standards

Conflict of interest

All authors claim that there are no conflicts of interest.

References

  1. 1.
    Amarenco P, Lavallee PC, Labreuche J, Albers GW, Bornstein NM, Canhao P, et al. One-year risk of stroke after transient ischemic attack or minor stroke. N Engl J Med 2016, 374: 1533–1542.CrossRefGoogle Scholar
  2. 2.
    Wang L, Jia J, Wu L. The relationship between cognitive impairment and cerebral blood flow changes after transient ischaemic attack. Neurol Res 2013, 35: 580–585.CrossRefGoogle Scholar
  3. 3.
    Turner GM, Calvert M, Feltham MG, Ryan R, Marshall T. Ongoing impairments following transient ischaemic attack: retrospective cohort study. Eur J Neurol 2016, 23: 1642–1650.CrossRefGoogle Scholar
  4. 4.
    van Rooij FG, Kessels RP, Richard E, De Leeuw FE, van Dijk EJ. Cognitive impairment in transient ischemic attack patients: a systematic review. Cerebrovasc Dis 2016, 42: 1–9.CrossRefGoogle Scholar
  5. 5.
    Balconi M. Dorsolateral prefrontal cortex, working memory and episodic memory processes: insight through transcranial magnetic stimulation techniques. Neurosci Bull 2013, 29: 381–389.CrossRefGoogle Scholar
  6. 6.
    Chen CJ, Chen CC, Wu D, Chi NF, Chen PC, Liao YP, et al. Effects of the apolipoprotein E epsilon4 allele on functional MRI during n-back working memory tasks in healthy middle-aged adults. AJNR Am J Neuroradiol 2013, 34: 1197–1202.CrossRefGoogle Scholar
  7. 7.
    Constantinidis C, Klingberg T. The neuroscience of working memory capacity and training. Nat Rev Neurosci 2016, 17: 438–449.CrossRefGoogle Scholar
  8. 8.
    Ziemus B, Baumann O, Luerding R, Schlosser R, Schuierer G, Bogdahn U, et al. Impaired working-memory after cerebellar infarcts paralleled by changes in BOLD signal of a cortico-cerebellar circuit. Neuropsychologia 2007, 45: 2016–2024.CrossRefGoogle Scholar
  9. 9.
    Umarova RM, Nitschke K, Kaller CP, Kloppel S, Beume L, Mader I, et al. Predictors and signatures of recovery from neglect in acute stroke. Ann Neurol 2016, 79: 673–686.CrossRefGoogle Scholar
  10. 10.
    Purcell J, Sebastian R, Leigh R, Jarso S, Davis C, Posner J, et al. Recovery of orthographic processing after stroke: A longitudinal fMRI study. Cortex 2017, 92: 103–118.CrossRefGoogle Scholar
  11. 11.
    Guo J, Chen N, Li R, Wu Q, Chen H, Gong Q, et al. Regional homogeneity abnormalities in patients with transient ischaemic attack: a resting-state fMRI study. Clin Neurophysiol 2014, 125: 520–525.CrossRefGoogle Scholar
  12. 12.
    Thermenos HW, Goldstein JM, Buka SL, Poldrack RA, Koch JK, Tsuang MT, et al. The effect of working memory performance on functional MRI in schizophrenia. Schizophr Res 2005, 74: 179–194.CrossRefGoogle Scholar
  13. 13.
    Sweet LH, Paskavitz JF, Haley AP, Gunstad JJ, Mulligan RC, Nyalakanti PK, et al. Imaging phonological similarity effects on verbal working memory. Neuropsychologia 2008, 46: 1114–1123.CrossRefGoogle Scholar
  14. 14.
    Walsh ND, Williams SC, Brammer MJ, Bullmore ET, Kim J, Suckling J, et al. A longitudinal functional magnetic resonance imaging study of verbal working memory in depression after antidepressant therapy. Biol Psychiatry 2007, 62: 1236–1243.CrossRefGoogle Scholar
  15. 15.
    Dobbins IG, Foley H, Schacter DL, Wagner AD. Executive control during episodic retrieval: multiple prefrontal processes subserve source memory. Neuron 2002, 35: 989–996.CrossRefGoogle Scholar
  16. 16.
    Goldman-Rakic PS. Working memory dysfunction in schizophrenia. J Neuropsychiatry Clin Neurosci 1994, 6: 348–357.CrossRefGoogle Scholar
  17. 17.
    Owen AM. The functional organization of working memory processes within human lateral frontal cortex: the contribution of functional neuroimaging. Eur J Neurosci 1997, 9: 1329–1339.CrossRefGoogle Scholar
  18. 18.
    Ku Y, Bodner M, Zhou YD. Prefrontal cortex and sensory cortices during working memory: quantity and quality. Neurosci Bull 2015, 31: 175–182.CrossRefGoogle Scholar
  19. 19.
    Callicott JH, Mattay VS, Bertolino A, Finn K, Coppola R, Frank JA, et al. Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. Cereb Cortex 1999, 9: 20–26.CrossRefGoogle Scholar
  20. 20.
    Marvel CL, Desmond JE. Functional topography of the cerebellum in verbal working memory. Neuropsychol Rev 2010, 20: 271–279.CrossRefGoogle Scholar
  21. 21.
    Chen L, Li C, Zhai J, Wang A, Song Q, Liu Y, et al. Altered resting-state signals in patients with acute stroke in or under the thalamus. Neurosci Bull 2016, 32: 585–590.CrossRefGoogle Scholar
  22. 22.
    Edwards JD, Meehan SK, Levy AR, Teal PA, Linsdell MA, Boyd LA. Changes in intracortical excitability after transient ischemic attack are associated with ABCD2 score. Stroke 2011, 42: 728–733.CrossRefGoogle Scholar
  23. 23.
    Koerner C, Meinck HM. Long-lasting motor cortex disinhibition after short transient ischemic attacks (TIAs) in humans. Neurosci Lett 2004, 361: 21–24.CrossRefGoogle Scholar
  24. 24.
    Burianova H, McIntosh AR, Grady CL. A common functional brain network for autobiographical, episodic, and semantic memory retrieval. Neuroimage 2010, 49: 865–874.CrossRefGoogle Scholar
  25. 25.
    Kornblith S, Quian Quiroga R, Koch C, Fried I, Mormann F. Persistent single-neuron activity during working memory in the human medial temporal lobe. Curr Biol 2017, 27: 1026–1032.CrossRefGoogle Scholar
  26. 26.
    Eryilmaz H, Tanner AS, Ho NF, Nitenson AZ, Silverstein NJ, Petruzzi LJ, et al. Disrupted working memory circuitry in schizophrenia: Disentangling fMRI markers of core pathology vs other aspects of impaired performance. Neuropsychopharmacology 2016, 41: 2411–2420.CrossRefGoogle Scholar
  27. 27.
    Tanaka S, Seki K, Hanakawa T, Harada M, Sugawara SK, Sadato N, et al. Abacus in the brain: a longitudinal functional MRI study of a skilled abacus user with a right hemispheric lesion. Front Psychol 2012, 3: 315.PubMedPubMedCentralGoogle Scholar
  28. 28.
    O’Brien JT, Erkinjuntti T, Reisberg B, Roman G, Sawada T, Pantoni L, et al. Vascular cognitive impairment. Lancet Neurol 2003, 2: 89–98.CrossRefGoogle Scholar
  29. 29.
    Cummings JL. Frontal-subcortical circuits and human behavior. Arch Neurol 1993, 50: 873–880.CrossRefGoogle Scholar
  30. 30.
    Sachdev PS, Brodaty H, Valenzuela MJ, Lorentz L, Looi JC, Wen W, et al. The neuropsychological profile of vascular cognitive impairment in stroke and TIA patients. Neurology 2004, 62: 912–919.CrossRefGoogle Scholar
  31. 31.
    Guyomard V, Metcalf AK, Naguib MF, Fulcher RA, Potter JF, Myint PK. Transient ischaemic attack, vascular risk factors and cognitive impairment: a case-controlled study. Age Ageing 2011, 40: 641–644.CrossRefGoogle Scholar
  32. 32.
    Winhuisen L, Thiel A, Schumacher B, Kessler J, Rudolf J, Haupt WF, et al. Role of the contralateral inferior frontal gyrus in recovery of language function in poststroke aphasia: a combined repetitive transcranial magnetic stimulation and positron emission tomography study. Stroke 2005, 36: 1759–1763.CrossRefGoogle Scholar
  33. 33.
    Friedmann N, Gvion A. Sentence comprehension and working memory limitation in aphasia: a dissociation between semantic-syntactic and phonological reactivation. Brain Lang 2003, 86: 23–39.CrossRefGoogle Scholar
  34. 34.
    Philipose LE, Alphs H, Prabhakaran V, Hillis AE. Testing conclusions from functional imaging of working memory with data from acute stroke. Behav Neurol 2007, 18: 37–43.CrossRefGoogle Scholar
  35. 35.
    Myerson J, Hale S, Rhee SH, Jenkins L. Selective interference with verbal and spatial working memory in young and older adults. J Gerontol B Psychol Sci Soc Sci 1999, 54: P161–164.CrossRefGoogle Scholar
  36. 36.
    den Heijer T, Geerlings MI, Hoebeek FE, Hofman A, Koudstaal PJ, Breteler MM. Use of hippocampal and amygdalar volumes on magnetic resonance imaging to predict dementia in cognitively intact elderly people. Arch Gen Psychiatry 2006, 63: 57–62.CrossRefGoogle Scholar

Copyright information

© Shanghai Institutes for Biological Sciences, CAS and Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Wei Su
    • 1
    • 2
  • Jian Guo
    • 1
  • Yun Zhang
    • 3
  • Jie Zhou
    • 1
  • Ning Chen
    • 1
  • Muke Zhou
    • 1
  • Rong Li
    • 4
  • Huafu Chen
    • 4
  • Li He
    • 1
    Email author
  1. 1.Department of NeurologyWest China Hospital of Sichuan UniversityChengduChina
  2. 2.Department of Science and TechnologyWest China Hospital of Sichuan UniversityChengduChina
  3. 3.Department of NeurologyMianyang Central HospitalMianyangChina
  4. 4.Key Laboratory for Neuroinformation of The Ministry of Education, School of Life Science and TechnologyUniversity of Electronic Science and Technology of ChinaChengduChina

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