Fractal dimension of EEG activity senses neuronal impairment in acute stroke

Abstract

The brain is a self-organizing system which displays self-similarities at different spatial and temporal scales. Thus, the complexity of its dynamics, associated to efficient processing and functional advantages, is expected to be captured by a measure of its scale-free (fractal) properties. Under the hypothesis that the fractal dimension (FD) of the electroencephalographic signal (EEG) is optimally sensitive to the neuronal dysfunction secondary to a brain lesion, we tested the FD's ability in assessing two key processes in acute stroke: the clinical impairment and the recovery prognosis. Resting EEG was collected in 36 patients 4-10 days after a unilateral ischemic stroke in the middle cerebral artery territory and 19 healthy controls. National Health Institute Stroke Scale (NIHss) was collected at T0 and 6 months later. Highuchi FD, its inter-hemispheric asymmetry (FDasy) and spectral band powers were calculated for EEG signals. FD was smaller in patients than in controls (1.447±0.092 vs 1.525±0.105) and its reduction was paired to a worse acute clinical status. FD decrease was associated to alpha increase and beta decrease of oscillatory activity power. Larger FDasy in acute phase was paired to a worse clinical recovery at six months. FD in our patients captured the loss of complexity reflecting the global system dysfunction resulting from the structural damage. This decrease seems to reveal the intimate nature of structure-function unity, where the regional neural multi-scale self-similar activity is impaired by the anatomical lesion. This picture is coherent with neuronal activity complexity decrease paired to a reduced repertoire of functional abilities. FDasy result highlights the functional relevance of the balance between homologous brain structures' activities in stroke recovery.

Figure 1. Topography of Fractal Dimension and relationship with clinical status and recovery.

A. Topographies of mean values of fractal dimension in the 3 groups: patients with lesion in left hemisphere (left), healthy age-matched controls (center), patients with lesion in right hemisphere (right). EEG electrodes are signed by a full circle. Left: mean and standard deviation of fractal dimension, averaged over all sensors of left (Fp1, F3, F7, T3, C3, T5, P3, O1) and right hemisphere (Fp2, F4, F8, T4, C4, T6, P4, O2), in the 3 groups (patients with the lesion in the left hemisphere, patients with the lesion in the right hemisphere, healthy controls). Center: scatter-plot of fractal dimension values over NIHss at T0 and fitting line. Right: scatter-plot of inter-hemispheric asymmetry index of fractal dimension values over effective recovery and fitting line. To be noted that negative values of asymmetry index denote FD values lower in the lesioned hemisphere than in the non-lesioned one.