Tong Mo1, Kan Deng2, Xiaoyu Wang1, Xiance Zhao3, Yijiang Zhuang1, Jieqiong Lin1, and Hongwu Zeng1
1Department of Radiology, Shenzhen Children’s Hospital, Shenzhen, China, 2Philips Healthcare, Guangzhou, China, 3Philips Healthcare, Shanghai, China
Synopsis
Keywords: Epilepsy, fMRI (resting state)
Motivation: The micro-structure alteration related to cognitive function impairment, and the mechanism of functional impairment in children withESES remains unclear.
Goal(s): To investigate the brain activity in children with ESES, and the associations of the brain activity with cognitive performance.
Approach: We observed the ReHo difference between the ESES group and the HCs. And the correlation analysis was used to explore the relationship between Reho values and cognitive test.
Results: Compared with HCs, patients with ESES showed ReHo alteration in some brain regions. The correlation analysis revealed that increased ReHo in the right frontal gyrus was correlated with the decreased PRI.
Impact: The distinct changes of spontaneous brain
activity were measured by ReHo, which may be further suggest that the potential
of RS-fMRI as a novel biomarker tool for identifying cognitive impairments on
neural aspect.
Introduction
Electrical Status Epilepticus During Sleep
(ESES) is a special EEG phenomenon that occurs in the process of sleep,
especially in the Non-Rapid Eye Movement (NREM). It was characterized by the
presence of focal or extensive persistent spike slow waves [1]. Previous
research result drew the conclusion that children with
ESES get cognitive function impairments and poor prognosis. However, the micro-structure alteration related to cognitive function
impairment, and the mechanism of functional impairment remains unclear. In
this study, we aimed to investigate the brain activity in children with ESES,
and the associations of the brain activity with cognitive performance.Methods
Twenty-five children with ESES, including
13 boys and 12 girls, aging from 6.75 to 12.33 years old (mean: 8.571.99
years), and 16 gender and age matched healthy controls (HCs)
were enrolled in this study. Resting state fMRI (rs-fMRI) data were acquired on
a 3.0T MRI system (Ingenia, Philips Healthcare, Best, the Netherlands). Then,
the rs-fMRI data preprocessing was carried out using the toolbox Data
Processing & Analysis for Brain Imaging (DPABI) [2]. The
regional homogeneity (ReHo) was calculated to characterize the local
synchronization of spontaneous brain activity. Wechsler
Intelligence scale for children-Fourth Edition (WISC-Ⅳ) was used for cognitive
test. The difference between the ESES group and the HCs were detected
using the two-sample t test. And the correlation analysis
was used to explore the
relationship between Reho values and cognitive test.Results
In cognitive test, patients with ESES
exhibited significant lower scores in Full-Scale Intelligence Quotient (FSIQ),
Comprehension Index (VCI) and Perceptual Reasoning Index (PRI) (P values
were 0.007, 0.034 and 0.008, respectively) compared with HCs (Tabel 1). Moreover,
compared with HCs, patients with ESES also showed decreased ReHo in left
postcentral gyrus, right superior temporal gyrus, right supplementary motor
area, right cerebellar lobule Ⅵ, right precentral gyrus and increased ReHo in
bilateral middle occipital gyrus, left middle frontal gyrus, left lingual gyrus,
cerebellar hemisphere Crus1 area and Crus2 area (Figure 1). The further correlation
analysis revealed that increased ReHo in the right frontal gyrus was positively
correlated with the decreased PRI (r = 0.761; P = 0.028). Discussion
In this study, the cognitive test showed
that patients with ESES have cognitive impairment in language, perceptual and
reasoning abilities. In addition, we identified synchronization of neural
activities alterations compared with the HC group. The cortex-cerebellar system
has been well documented in humans and primates, with separate and closed
circuits between the cerebellum and cortex. Middleton, Kelly and Strick et al. [3,
4] discovered two cortical-cerebellar circuits: the motor circuit and the
frontal circuit. In the motor circuit, the primary motor cortex projects
signals to the V, VI, HVIIB and HVIII parts of the cerebellar cortex, and then
returns to the primary motor cortex through the dorsal cerebellar dentate
nucleus and thalamus. In the prefrontal loop, area 46 of the prefrontal cortex
projects information through the pontine nucleus to the HVIIA part of the
cerebellar cortex lobules (mainly Crus1 and Crus2 areas), and then returns to
the prefrontal cortex through the ventral dentate nucleus and thalamus of the
cerebellum [5-7]. Therefore, cerebellum Cru1 and Crus2 regions are
closely related to the functions of the prefrontal cortex. Language function of
ESES group was impaired compared with the normal control group, while Crus1 and
Crus2 the ReHo values had increased. We might get the conclusion that the
language centers of the cerebral hemisphere and the language activation areas
of the cerebellum have a synergistic effect. When the function of the language
centers of the brain declines, the language function of Cru1 and Crus2 regions
may increase compensatively, or some of the language function of the brain may
shift to the cerebellum. This is consistent with the findings of Lin et al. [8]
that the ReHo value in the cerebral hemisphere decreased and the ReHo value in
the cerebellum increased compensatively in patients with cirrhosis. These
compensatory changes may be related to the redistribution of blood flow and
metabolism [9, 10].Conclusion
Cognitive test showed cognitive impairments
in patients with ESES. The distinct changes of spontaneous brain activity were measured
by ReHo, which may be further suggest that the potential of RS-fMRI as a novel
biomarker tool for identifying cognitive impairments on neural aspect.Acknowledgements
We would like to acknowledge the generous support and contribution of all our trial participants.References
[1]
Patry G, Lyagoubi S, Tassinari CA. Subclinical "electrical
status epilepticus" induced by sleep in children. A clinical and
electroencephalographic study of six cases. Arch Neurol. 1971. 24(3): 242-52.
[2] Yan, CG., Wang, XD., Zuo, XN. et al. DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging. Neuroinform 14, 339–351 (2016).
[3]
Middleton FA, Strick PL. Basal ganglia and cerebellar loops: motor and
cognitive circuits. Brain Res Brain Res Rev. 2000. 31(2-3): 236-50.
[4]
Kelly RM, Strick PL. Cerebellar loops with motor cortex and prefrontal cortex
of a nonhuman primate. J Neurosci. 2003. 23(23): 8432-44.
[5]
Middleton FA, Strick PL. Cerebellar projections to the prefrontal cortex of the
primate. J Neurosci. 2001. 21(2): 700-12.
[6]
Barbas H, Henion TH, Dermon CR. Diverse thalamic projections
to the prefrontal cortex in the rhesus monkey. J Comp Neurol. 1991. 313(1):
65-94.
[7]
Goldman-Rakic PS, Porrino LJ. The primate mediodorsal (MD)
nucleus and its projection to the frontal lobe. J Comp Neurol. 1985. 242(4):
535-60.
[8]
Lin WC, Hsu TW, Chen CL, Lu CH, Chen HL, Cheng YF. Resting State-fMRI with ReHo Analysis as a Non-Invasive
Modality for the Prognosis of Cirrhotic Patients with Overt Hepatic
Encephalopathy. PLoS One. 2015. 10(5): e0126834.
[9]
Lockwood AH, Yap EW, Wong WH. Cerebral ammonia metabolism in patients with
severe liver disease and minimal hepatic encephalopathy. J Cereb Blood Flow Metab. 1991. 11(2): 337-41.
[10] Ahl B, Weissenborn
K, van den Hoff J, et al. Regional differences in cerebral blood flow and
cerebral ammonia metabolism in patients with cirrhosis. Hepatology. 2004.
40(1): 73-9.