Skip to main content
SpringerLink
Log in

Effective connectivity alteration according to recurrence in transient global amnesia

  • Diagnostic Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

This study aimed to evaluate alterations in structural covariance network and effective connectivity of the intrahippocampal circuit in patients with transient global amnesia (TGA). We also investigated whether there were differences of them according to recurrence.

Methods

We enrolled 88 patients with TGA and 50 healthy controls. We classified patients with TGA into two groups: the single event group (N = 77) and recurrent events group (N = 11). We performed volumetric analysis using the FreeSurfer program and structural covariance network analysis based on the structural volumes using a graph theoretical analysis in patients with TGA and healthy controls. The effective connectivity of the intrahippocampal circuit was also evaluated using structural equation modeling.

Results

There were no significant differences between patients with all TGA events/a single TGA event and healthy controls with regard to global structural covariance network. However, patients with recurrent events had significant alterations in global structural covariance network with a decrease in the small-worldness index (0.907 vs. 0.970, p = 0.032). In patients with all events/a single, there were alterations in effective connectivity from the entorhinal cortex to CA4, only. However, in patients with recurrent events, there were alterations in effective connectivity from the subiculum to the fimbria as well as from the entorhinal cortex to CA4 in bilateral hemispheres.

Conclusion

Our study revealed significant alterations in structural covariance network and disruption of the intrahippocampal circuit in patients with TGA compared to healthy controls, which is more prominent when amnestic events recurred. It could be related to the pathogenesis of TGA.

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

Similar content being viewed by others

Data Availability

Data that support the findings of this study are available upon reasonable request.

References

  1. Bartsch T, Deuschl G (2010) Transient global amnesia: functional anatomy and clinical implications. Lancet Neurol 9(2):205–214

    Article  Google Scholar 

  2. Lewis SL (1998) Aetiology of transient global amnesia. Lancet 352(9125):397–399

    Article  CAS  Google Scholar 

  3. Sander K, Sander D (2005) New insights into transient global amnesia: recent imaging and clinical findings. Lancet Neurol 4(7):437–444

    Article  Google Scholar 

  4. Arena JE, Brown RD, Mandrekar J, Rabinstein AA (2017) Long-term outcome in patients with transient global amnesia: a population-based study. In: Mayo Clinic Proceedings. vol 3. Elsevier, pp 399–405

  5. Ikegaya Y, Matsuki N (2002) Regionally selective neurotoxicity of NMDA and colchicine is independent of hippocampal neural circuitry. Neuroscience 113(2):253–256

    Article  CAS  Google Scholar 

  6. Joëls M (2009) Stress, the hippocampus, and epilepsy. Epilepsia 50(4):586–597

    Article  Google Scholar 

  7. Bartsch T, Alfke K, Stingele R, Rohr A, Freitag-Wolf S, Jansen O, Deuschl G (2006) Selective affection of hippocampal CA-1 neurons in patients with transient global amnesia without long-term sequelae. Brain 129(11):2874–2884

    Article  CAS  Google Scholar 

  8. Squire LR, Stark CE, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306

    Article  CAS  Google Scholar 

  9. Bartsch T, Alfke K, Deuschl G, Jansen O (2007) Evolution of hippocampal CA-1 diffusion lesions in transient global amnesia. Ann Neurol 62(5):475–480

    Article  Google Scholar 

  10. Friston KJ (2011) Functional and effective connectivity: a review. Brain Connect 1(1):13–36

    Article  Google Scholar 

  11. Karwowski W, Vasheghani Farahani F, Lighthall N (2019) Application of graph theory for identifying connectivity patterns in human brain networks: a systematic review. frontiers in. Neuroscience 13:585

    Google Scholar 

  12. Coben R, Mohammad-Rezazadeh I (2015) Neural connectivity in epilepsy as measured by Granger causality. Front Hum Neurosci 9:194

    Article  Google Scholar 

  13. Laird AR, Robbins JM, Li K, Price LR, Cykowski MD, Narayana S, Laird RW, Franklin C, Fox PT (2008) Modeling motor connectivity using TMS/PET and structural equation modeling. Neuroimage 41(2):424–436

    Article  Google Scholar 

  14. Park KM, Lee BI, Shin KJ, Ha SY, Park J, Kim SE, Kim HC, Kim TH, Mun CW, Kim SE (2017) Juvenile myoclonic epilepsy may be a disorder of cortex rather than thalamus: an effective connectivity analysis. J Clin Neurosci 35:127–132

    Article  Google Scholar 

  15. Hodges J, Warlow C (1990) Syndromes of transient amnesia: towards a classification. A study of 153 cases. J Neurol Neurosurg Psychiatry 53(10):834–843

    Article  CAS  Google Scholar 

  16. Quinette P, Guillery-Girard B, Dayan J, Vdl S, Marquis S, Viader F, Desgranges B, Eustache F (2006) What does transient global amnesia really mean? Review of the literature and thorough study of 142 cases. Brain 129(7):1640–1658

    Article  Google Scholar 

  17. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, Van Der Kouwe A, Killiany R, Kennedy D, Klaveness S (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33(3):341–355

    Article  CAS  Google Scholar 

  18. Mijalkov M, Kakaei E, Pereira JB, Westman E, Volpe G, Initiative ADN (2017) BRAPH: a graph theory software for the analysis of brain connectivity. PLoS One 12(8):e0178798

    Article  Google Scholar 

  19. Lee DA, Kim BJ, Lee H-J, Kim SE, Park KM (2020) Network characteristics of genetic generalized epilepsy: are the syndromes distinct? Seizure 82:91–98

    Article  Google Scholar 

  20. Park K, Kim S, Shin K, Ha S, Park J, Kim T, Mun C, Lee B, Kim S (2017) Effective connectivity in temporal lobe epilepsy with hippocampal sclerosis. Acta Neurol Scand 135(6):670–676

    Article  CAS  Google Scholar 

  21. Park KM, Han YH, Kim TH, Mun CW, Shin KJ, Ha SY, Park J, Kim SE (2015) Pre-existing structural abnormalities of the limbic system in transient global amnesia. J Clin Neurosci 22(5):843–847

    Article  Google Scholar 

  22. Kim HC, Lee BI, Kim SE, Park KM (2017) Cortical morphology in patients with transient global amnesia. Brain Behav 7(12):e00872

    Article  Google Scholar 

  23. Park KM, Lee BI, Kim SE (2018) Is transient global amnesia a network disease? Eur Neurol 80(5-6):345–354

    Article  Google Scholar 

  24. Hodel J, Leclerc X, Zuber M, Gerber S, Besson P, Marcaud V, Roubeau V, Brasme H, Ganzoui I, Ducreux D (2020) Structural connectivity and cortical thickness alterations in transient global amnesia. Am J Neuroradiol 41(5):798–803

    Article  CAS  Google Scholar 

  25. Bernhardt B, Hong S-J, Bernasconi A, Bernasconi N (2013) Imaging structural and functional brain networks in temporal lobe epilepsy. Front Hum Neurosci 7:624

    Article  Google Scholar 

  26. Ueda I, Takemoto K, Watanabe K, Sugimoto K, Ikenouchi A, Kakeda S, Katsuki A, Yoshimura R, Korogi Y (2020) The brain-derived neurotrophic factor Val66Met polymorphism increases segregation of structural correlation networks in healthy adult brains. PeerJ 8:e9632

    Article  Google Scholar 

  27. Kakeda S, Watanabe K, Nguyen H, Katsuki A, Sugimoto K, Igata N, Abe O, Yoshimura R, Korogi Y (2020) An independent component analysis reveals brain structural networks related to TNF-α in drug-naïve, first-episode major depressive disorder: a source-based morphometric study. Transl Psychiatry 10(1):1–7

    Article  Google Scholar 

  28. Duarte A, Henson RN, Knight RT, Emery T, Graham KS (2010) Orbito-frontal cortex is necessary for temporal context memory. J Cogn Neurosci 22(8):1819–1831

    Article  Google Scholar 

  29. Frank LE, Preston AR, Zeithamova D (2019) Functional connectivity between memory and reward centers across task and rest track memory sensitivity to reward. Cogn Affect Behav Neurosci 19(3):503–522

    Article  Google Scholar 

  30. Jeneson A, Squire LR (2012) Working memory, long-term memory, and medial temporal lobe function. Learn Mem 19(1):15–25

    Article  Google Scholar 

  31. Basu J, Siegelbaum SA (2015) The corticohippocampal circuit, synaptic plasticity, and memory. Cold Spring Harb Perspect Biol 7(11):a021733

    Article  Google Scholar 

  32. Knierim JJ, Lee I, Hargreaves EL (2006) Hippocampal place cells: parallel input streams, subregional processing, and implications for episodic memory. Hippocampus 16(9):755–764

    Article  Google Scholar 

  33. Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA (2011) A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 12(10):585–601

    Article  CAS  Google Scholar 

  34. Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6(10):2950–2967

    Article  CAS  Google Scholar 

  35. Conrad CD, Roy EJ (1993) Selective loss of hippocampal granule cells following adrenalectomy: implications for spatial memory. J Neurosci 13(6):2582–2590

    Article  CAS  Google Scholar 

  36. Bakker A, Kirwan CB, Miller M, Stark CE (2008) Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319(5870):1640–1642

    Article  CAS  Google Scholar 

  37. Viskontas IV, Carr VA, Engel SA, Knowlton BJ (2009) The neural correlates of recollection: hippocampal activation declines as episodic memory fades. Hippocampus 19(3):265–272

    Article  Google Scholar 

Download references

Acknowledgments

None

Funding

This study has not been funded.

Author information

Author notes

  1. DAL and SL equally contributed to this article.

Authors and Affiliations

  1. Department of Neurology, Haeundae Paik Hospital, Inje University College of Medicine, Haeundae-ro 875, Haeundae-gu, Busan, Republic of Korea

    Dong Ah Lee & Kang Min Park

  2. Department of Neurosurgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea

    Sungjoon Lee

  3. Department of Ship Design & Engineering, Korea Research Institute of Ships & Ocean Engineering, Busan, Republic of Korea

    Due Won Kim

  4. Department of Radiology, Haeundae Paik Hospital, Inje University College of Medicine, Busan, Republic of Korea

    Ho-Joon Lee

Authors
  1. Dong Ah Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sungjoon Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Due Won Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ho-Joon Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kang Min Park
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kang Min Park.

Ethics declarations

Conflicts of interest

We declare that we have no conflict of interest.

Ethical approval

All procedures performed in the 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.

Code availability

Not applicable

Additional information

Publisher’s note

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

Supplementary information

ESM 1

(PDF 179 kb)

ESM 2

(PDF 40.1 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, D.A., Lee, S., Kim, D.W. et al. Effective connectivity alteration according to recurrence in transient global amnesia. Neuroradiology 63, 1441–1449 (2021). https://doi.org/10.1007/s00234-021-02645-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-021-02645-7

Keywords

Search

Navigation