EEG and Neuronal Activity Topography analysis can predict effectiveness of shunt operation in idiopathic normal pressure hydrocephalus patients

Abstract

Idiopathic normal pressure hydrocephalus (iNPH) is a neuropsychiatric syndrome characterized by gait disturbance, cognitive impairment and urinary incontinence that affect elderly individuals. These symptoms can potentially be reversed by cerebrospinal fluid (CSF) drainage or shunt operation. Prior to shunt operation, drainage of a small amount of CSF or “CSF tapping” is usually performed to ascertain the effect of the operation. Unfortunately, conventional neuroimaging methods such as single photon emission computed tomography (SPECT) and functional magnetic resonance imaging (fMRI), as well as electroencephalogram (EEG) power analysis seem to have failed to detect the effect of CSF tapping on brain function. In this work, we propose the use of Neuronal Activity Topography (NAT) analysis, which calculates normalized power variance (NPV) of EEG waves, to detect cortical functional changes induced by CSF tapping in iNPH. Based on clinical improvement by CSF tapping and shunt operation, we classified 24 iNPH patients into responders (N = 11) and nonresponders (N = 13), and performed both EEG power analysis and NAT analysis. We also assessed correlations between changes in NPV and changes in functional scores on gait and cognition scales before and after CSF tapping. NAT analysis showed that after CSF tapping there was a significant decrease in alpha NPV at the medial frontal cortex (FC) (Fz) in responders, while nonresponders exhibited an increase in alpha NPV at the right dorsolateral prefrontal cortex (DLPFC) (F8). Furthermore, we found correlations between cortical functional changes and clinical symptoms. In particular, delta and alpha NPV changes in the left-dorsal FC (F3) correlated with changes in gait status, while alpha and beta NPV changes in the right anterior prefrontal cortex (PFC) (Fp2) and left DLPFC (F7) as well as alpha NPV changes in the medial FC (Fz) correlated with changes in gait velocity. In addition, alpha NPV changes in the right DLPFC (F8) correlated with changes in WMS-R Mental Control scores in iNPH patients. An additional analysis combining the changes in values of alpha NPV over the left-dorsal FC (∆alpha-F3-NPV) and the medial FC (∆alpha-Fz-NPV) induced by CSF tapping (cut-off value of ∆alpha-F3-NPV + ∆alpha-Fz-NPV = 0), could correctly identified “shunt responders” and “shunt nonresponders” with a positive predictive value of 100% (10/10) and a negative predictive value of 66% (2/3). In contrast, EEG power spectral analysis showed no function related changes in cortical activity at the frontal cortex before and after CSF tapping. These results indicate that the clinical changes in gait and response suppression induced by CSF tapping in iNPH patients manifest as NPV changes, particularly in the alpha band, rather than as EEG power changes. Our findings suggest that NAT analysis can detect CSF tapping-induced functional changes in cortical activity, in a way that no other neuroimaging methods have been able to do so far, and can predict clinical response to shunt operation in patients ...

Noninvasive prediction of shunt operation outcome in idiopathic normal pressure hydrocephalus

“…Allali et al, using the walking test in dual task conditions, have reported that after CSF tapping iNPH patients significantly improved allocation of attention to gait during dual task 21 , which is a function of right VAN 17 22 , compared to iNPH-like patients. Also, in a previous study, we found that alpha and beta NPV changes at the right anterior prefrontal electrode (Fp2) correlated with changes in walking time, which suggests a recruitment of the right VAN in gait control in iNPH patients 8 . This recruitment of VAN during gait has also been seen in patients with Parkinson's disease, and these authors discussed that an associated burn-out of VAN may lead to the freezing of gait 23 .…”

“…More specifically, improvement of walking time attributed to CSF tapping correlated with an alpha NPV decrease in the supplementary motor area (SMA) and alpha and beta NPV decreases in the prefrontal cortices (PFC), especially in the right anterior PFC. In addition, gait status recovery correlated with delta and alpha NPV decreases in the left dorsal premotor area (PMA), and attention recovery correlated with an alpha NPV decrease in the right dorsolateral PFC (DLPFC) 8 . These findings demonstrated the important involvement of the right anterior PFC and premotor cortex to gait improvement induced by CSF tapping in iNPH patients.…”

“…EEG has become a useful tool in neuroscience to investigate cortical functions 8 , and also in clinical practice for objective clinical assessment of neurological and neuropsychiatric disorders, such as epilepsy and Alzheimer's disease 11 . This usefulness mainly arises from the fact that EEG can directly measure brain electrical activity 12 13 .…”

Healthy and Pathological Brain Aging: From the Perspective of Oscillations, Functional Connectivity, and Signal Complexity

“…NAT is a novel analysis method that measures EEG normalized power variance (NPV), an index of waveform complexity [76]. This method has been used successfully to detect changes in the complexity of signal dynamics associated with cognitive and clinical improvement in patients with normal pressure hydrocephalus who respond to shunt operation [77]. It was also reported that an NPV decrease represents the stabilization of cortical electrical activity which reflects functional improvement, while an NPV increase represents the destabilization of cortical electrical activity which reflects functional worsening [77].…”

“…This method has been used successfully to detect changes in the complexity of signal dynamics associated with cognitive and clinical improvement in patients with normal pressure hydrocephalus who respond to shunt operation [77]. It was also reported that an NPV decrease represents the stabilization of cortical electrical activity which reflects functional improvement, while an NPV increase represents the destabilization of cortical electrical activity which reflects functional worsening [77]. In our study, NAT results showed an increase in NPV values from younger to middle-aged subjects, and a decrease in the values from middle-aged to the elderly, after an analysis of all regions and locations.…”