Reversible functional connectivity disturbances during transient global amnesia
Michael Peer MSc
Department of Neurology, Hadassah Hebrew University Medical School, Jerusalem, Israel
Faculty of Medicine, Hadassah Hebrew University Medical School, Jerusalem, Israel
Search for more papers by this authorMor Nitzan MSc
Faculty of Medicine, Hadassah Hebrew University Medical School, Jerusalem, Israel
Racah Institute of Physics, Hebrew University of Jerusalem, Jerusalem, Israel
Search for more papers by this authorIlan Goldberg MD, PhD
Department of Neurology, Hadassah Hebrew University Medical School, Jerusalem, Israel
Faculty of Medicine, Hadassah Hebrew University Medical School, Jerusalem, Israel
Search for more papers by this authorJudith Katz
Department of Neurology, Hadassah Hebrew University Medical School, Jerusalem, Israel
Search for more papers by this authorJ. Moshe Gomori MD
Department of Radiology, Hadassah Hebrew University Medical Center, Jerusalem, Israel
Search for more papers by this authorTamir Ben-Hur MD, PhD
Department of Neurology, Hadassah Hebrew University Medical School, Jerusalem, Israel
Faculty of Medicine, Hadassah Hebrew University Medical School, Jerusalem, Israel
Search for more papers by this authorCorresponding Author
Shahar Arzy MD, PhD
Department of Neurology, Hadassah Hebrew University Medical School, Jerusalem, Israel
Faculty of Medicine, Hadassah Hebrew University Medical School, Jerusalem, Israel
Address correspondence to Dr Arzy, Neuropsychiatry Lab, Department of Neurology, Faculty of Medicine, Hadassah Hebrew University Medical School, Jerusalem, Israel. E-mail: [email protected]Search for more papers by this authorMichael Peer MSc
Department of Neurology, Hadassah Hebrew University Medical School, Jerusalem, Israel
Faculty of Medicine, Hadassah Hebrew University Medical School, Jerusalem, Israel
Search for more papers by this authorMor Nitzan MSc
Faculty of Medicine, Hadassah Hebrew University Medical School, Jerusalem, Israel
Racah Institute of Physics, Hebrew University of Jerusalem, Jerusalem, Israel
Search for more papers by this authorIlan Goldberg MD, PhD
Department of Neurology, Hadassah Hebrew University Medical School, Jerusalem, Israel
Faculty of Medicine, Hadassah Hebrew University Medical School, Jerusalem, Israel
Search for more papers by this authorJudith Katz
Department of Neurology, Hadassah Hebrew University Medical School, Jerusalem, Israel
Search for more papers by this authorJ. Moshe Gomori MD
Department of Radiology, Hadassah Hebrew University Medical Center, Jerusalem, Israel
Search for more papers by this authorTamir Ben-Hur MD, PhD
Department of Neurology, Hadassah Hebrew University Medical School, Jerusalem, Israel
Faculty of Medicine, Hadassah Hebrew University Medical School, Jerusalem, Israel
Search for more papers by this authorCorresponding Author
Shahar Arzy MD, PhD
Department of Neurology, Hadassah Hebrew University Medical School, Jerusalem, Israel
Faculty of Medicine, Hadassah Hebrew University Medical School, Jerusalem, Israel
Address correspondence to Dr Arzy, Neuropsychiatry Lab, Department of Neurology, Faculty of Medicine, Hadassah Hebrew University Medical School, Jerusalem, Israel. E-mail: [email protected]Search for more papers by this authorAbstract
Objective
Transient global amnesia (TGA), an abrupt occurrence of severe anterograde episodic amnesia accompanied by repetitive questioning, has been known for more than 50 years. Despite extensive research, there is no clear evidence for the underlying pathophysiological basis of TGA. Moreover, there is no neuroimaging method to evaluate TGA in real time.
Methods
Here we used resting-state functional magnetic resonance imaging recorded in 12 patients during the acute phase of TGA together with connectivity and cluster analyses to detect changes in the episodic memory network in TGA.
Results
Our results show a significant reduction in functional connectivity of the episodic memory network during TGA, which is more pronounced in the hyperacute phase than in the postacute phase. This disturbance is bilateral, and reversible after recovery. Although the hippocampus and its connections are significantly impaired, other parts of the episodic memory network are also impaired. Similar results were obtained for the analysis of the episodic memory network whether it was defined in a data-driven or literature-based manner.
Interpretation
These results suggest that TGA is related to a functional disturbance in the episodic memory network, and supply a neuroimaging correlate of TGA during the acute phase. Ann Neurol 2014;75:634–643
References
- 1 Hainselin M, Quinette P, Desgranges B, et al. Awareness of disease state without explicit knowledge of memory failure in transient global amnesia. Cortex 2012; 48: 1079–1084.
- 2 Hodges JR, Warlow CP. Syndromes of transient amnesia: towards a classification. A study of 153 cases. J Neurol Neurosurg Psychiatry 1990; 53: 834–843.
- 3 Hodges JR, Ward CD. Observations during transient global amnesia. A behavioural and neuropsychological study of five cases. Brain 1989; 112: 595–620.
- 4 Jäger T, Szabo K, Griebe M, et al. Selective disruption of hippocampus-mediated recognition memory processes after episodes of transient global amnesia. Neuropsychologia 2009; 47: 70–76.
- 5 Quinette P, Guillery-Girard B, Dayan J, et al. What does transient global amnesia really mean? Review of the literature and thorough study of 142 cases. Brain 2006; 129: 1640–1658.
- 6 Bartsch T, Deuschl G. Transient global amnesia: functional anatomy and clinical implications. Lancet Neurol 2010; 9: 205–214.
- 7 Baron JC, Petit-Taboué MC, Le Doze F, et al. Right frontal cortex hypometabolism in transient global amnesia. A PET study. Brain 1994; 117: 545–552.
- 8 Eustache F, Desgranges B, Petit-Taboué MC, et al. Transient global amnesia: implicit/explicit memory dissociation and PET assessment of brain perfusion and oxygen metabolism in the acute stage. J Neurol Neurosurg Psychiatry 1997; 63: 357–367.
- 9 Guillery B, Desgranges B, de la Sayette V, et al. Transient global amnesia: concomitant episodic memory and positron emission tomography assessment in two additional patients. Neurosci Lett 2002; 325: 62–66.
- 10 LaBar KS, Gitelman DR, Parrish TB, Mesulam MM. Functional changes in temporal lobe activity during transient global amnesia. Neurology 2002; 58: 638–641.
- 11 Westmacott R, Silver FL, McAndrews MP. Understanding medial temporal activation in memory tasks: evidence from fMRI of encoding and recognition in a case of transient global amnesia. Hippocampus 2008; 18: 317–325.
- 12 Sedlaczek O, Hirsch JG, Grips E, et al. Detection of delayed focal MR changes in the lateral hippocampus in transient global amnesia. Neurology 2004; 62: 2165–2170.
- 13 Bartsch T, Alfke K, Stingele R, et al. Selective affection of hippocampal CA-1 neurons in patients with transient global amnesia without long-term sequelae. Brain 2006; 129: 2874–2884.
- 14 Bartsch T, Alfke K, Deuschl G, Jansen O. Evolution of hippocampal CA-1 diffusion lesions in transient global amnesia. Ann Neurol 2007; 62: 475–480.
- 15 Lee HY, Kim JH, Weon YC, et al. Diffusion-weighted imaging in transient global amnesia exposes the CA1 region of the hippocampus. Neuroradiology 2007; 49: 481–487.
- 16 Corkin S. Lasting consequences of bilateral medial temporal lobectomy: clinical course and experimental findings in H.M. Semin Neurol 2008; 4: 249–259.
- 17 Zhang D, Raichle ME. Disease and the brain's dark energy. Nat Rev Neurol 2010; 6: 15–28.
- 18 Pievani M, de Haan W, Wu T, et al. Functional network disruption in the degenerative dementias. Lancet Neurol 2011; 10: 829–843.
- 19 Park C, Chang WH, Ohn SH, et al. Longitudinal changes of resting-state functional connectivity during motor recovery after stroke. Stroke 2011; 42: 1357–1362.
- 20 Chao-Gan Y, Yu-Feng Z. DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 2010; 4: 13.
- 21 Power JD, Barnes KA, Snyder AZ, et al. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 2012; 59: 2142–2154.
- 22 Satterthwaite TD, Wolf DH, Loughead J, et al. Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage 2012; 60: 623–632.
- 23 Van Dijk KRA, Sabuncu MR, Buckner RL. The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 2012; 59: 431–438.
- 24 Friston KJ, Williams S, Howard R, et al. Movement-related effects in fMRI time-series. Magn Reson Med 1996; 35: 346–355.
- 25 Satterthwaite TD, Elliott MA, Gerraty RT, et al. An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 2013; 64: 240–256.
- 26 Tzourio-Mazoyer N, Landeau B, Papathanassiou D, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002; 15: 273–289.
- 27 Deichmann R, Josephs O, Hutton C, et al. Compensation of susceptibility-induced BOLD sensitivity losses in echo-planar fMRI imaging. Neuroimage 2002; 15: 120–135.
- 28 Nadel L, Moscovitch M. Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol 1997; 7: 217–227.
- 29 Svoboda E, McKinnon MC, Levine B. The functional neuroanatomy of autobiographical memory: a meta-analysis. Neuropsychologia 2006; 44: 2189–2208.
- 30 Van Marle HJ, Hermans EJ, Qin S, Fernández G. Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress. Neuroimage 2010; 53: 348–354.
- 31 Veer IM, Oei NY, Spinhoven P, et al. Beyond acute social stress: increased functional connectivity between amygdala and cortical midline structures. Neuroimage 2011; 57: 1534–1541.
- 32 Schultz DH, Balderston NL, Helmstetter FJ. Resting-state connectivity of the amygdala is altered following Pavlovian fear conditioning. Front Hum Neurosci 2012; 6: 242.
- 33 Vaisvaser S, Lin T, Admon R, et al. Neural traces of stress: cortisol related sustained enhancement of amygdala-hippocampal functional connectivity. Front Hum Neurosci 2013; 7: 313.
- 34 Ashburner J, Friston KJ. Voxel-based morphometry—the methods. Neuroimage 2000; 11: 805–821.
- 35 Stillhard G, Landis T, Schiess R, et al. Bitemporal hypoperfusion in transient global amnesia: 99m-Tc-HM-PAO SPECT and neuropsychological findings during and after an attack. J Neurol Neurosurg Psychiatry 1990; 53: 339–342.
- 36 Di Filippo M, Calabresi P. Ischemic bilateral hippocampal dysfunction during transient global amnesia. Neurology 2007; 69: 493.
- 37 Shimamura AP. Hierarchical relational binding in the medial temporal lobe: the strong get stronger. Hippocampus 2010; 20: 1206–1216.
- 38 Markowitsch HJ, Staniloiu A. Amnesic disorders. Lancet 2012; 380: 1429–1440.
Citing Literature
