Preserved fractal character of structural brain networks is associated with covert consciousness after severe brain injury

Andrea I Luppi,Michael M Craig,Peter Coppola,Alexander R.D Peattie,Paola Finoia,Guy B Williams,Judith Allanson,John D Pickard,David K Menon,Emmanuel A Stamatakis

doi:10.1016/j.nicl.2021.102682

Abstract

Self-similarity is ubiquitous throughout natural phenomena, including the human brain. Recent evidence indicates that fractal dimension of functional brain networks, a measure of self-similarity, is diminished in patients diagnosed with disorders of consciousness arising from severe brain injury. Here, we set out to investigate whether loss of self-similarity is observed in the structural connectome of patients with disorders of consciousness. Using diffusion MRI tractography from N = 11 patients in a minimally conscious state (MCS), N = 10 patients diagnosed with unresponsive wakefulness syndrome (UWS), and N = 20 healthy controls, we show that fractal dimension of structural brain networks is diminished in DOC patients. Remarkably, we also show that fractal dimension of structural brain networks is preserved in patients who exhibit evidence of covert consciousness by performing mental imagery tasks during functional MRI scanning. These results demonstrate that differences in fractal dimension of structural brain networks are quantitatively associated with chronic loss of consciousness induced by severe brain injury, highlighting the close connection between structural organisation of the human brain and its ability to support cognitive function.

Highlights

Self-similarity is ubiquitous throughout natural phenomena – from the progressively branching structure of trees, rivers and blood vessels, to the human brain being a network composed of nested sub-networks
We compared weighted fractal dimension of structural brain net works across N = healthy controls and N = disorders of consciousness (DOC) patients belonging to different diagnostic categories (N = 11 minimally conscious state (MCS) and N = 10 unresponsive wake fulness syndrome/vegetative state (UWS))
Analysis of covariance indicated a significant effect of condition on weighted fractal dimension (FD): F(2,36) = 19.53, p < 0.001

Summary

Introduction

Self-similarity is ubiquitous throughout natural phenomena – from the progressively branching structure of trees, rivers and blood vessels, to the human brain being a network composed of nested sub-networks. Self-similarity across scales can be quantified in terms of fractal dimension, the extent that the same organisation can be observed across levels of detail, i.e. when considering the whole system or “zooming in” on its parts. Anatomi cally, fractal dimension of grey and white matter structures has been associated with cognitive outcomes – in the healthy brain, and in aging or disease (Im et al, 2006; King et al, 2009; Mustafa et al, 2012; Tae et al, 2005). Electroencephalography (EEG) and functional MRI can provide estimates of fractal dimension in both space and time, which have been shown to reflect cognitive performance (Bornas et al, 2013), the altered state of consciousness induced by psychedelics (Varley et al, 2020a) and loss of consciousness due to natural sleep or different anaesthetics (Ruiz de Miras et al, 2019; Varley et al, 2020c)

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