The neural basis of external responsiveness in prolonged disorders of consciousness.

Clara A Stafford,Adrian M Owen,Davinia Fernández-Espejo

doi:10.1016/j.nicl.2019.101791

Clara A Stafford, Adrian M Owen + Show 1 more

Open Access

https://doi.org/10.1016/j.nicl.2019.101791

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Abstract

ObjectiveTo investigate the structural integrity of fibre tracts underlying overt motor behaviour in PDOC.MethodsThis cross-sectional study examined 15 PDOC patients and 22 healthy participants. Eight PDOC patients met the criteria for the vegetative state, 5 met the criteria for the minimally conscious state and 2 met the criteria for emerging from the minimally conscious state. We used fibre tractography to reconstruct the white matter fibres known to be involved in voluntary motor execution (i.e., those connecting thalamus with M1, M1 with cerebellum, and cerebellum with thalamus) and used fractional anisotropy (FA) as a measure of their integrity.ResultsPDOC patients showed significantly reduced FA relative to controls on the fibres connecting thalamus and M1. This went above and beyond a widespread injury to the white matter and correlated with clinical severity. In a subset of patients, we also identified a similar pattern of injury in the fibres connecting M1 and cerebellum but a relative preservation of those connecting cerebellum and thalamus.ConclusionsOur results suggest that structural damage to motor fibres may lead to reduced responsiveness in PDOC patients across all diagnostic sub-categories, and therefore behavioural assessments may underestimate the level of retained cognitive function and awareness across the PDOC spectrum.

Highlights

The current gold-standard for diagnosing Prolonged Disorders of Consciousness (PDOC) is standardized behavioural scales (e.g., Coma Recovery Scale-Revised (CRS-R); Giacino and Kalmar, 2004), which require the patient to demonstrate their level of awareness through overt responses
Our results suggest that structural damage to motor fibres may lead to reduced responsiveness in PDOC patients across all diagnostic sub-categories, and behavioural assessments may underestimate the level of retained cognitive function and awareness across the PDOC spectrum
We showed that structural damage to the fibres connecting the thalamus and the primary motor cortex (M1) may be disrupting an excitatory coupling between these structures, which is necessary for motor execution it remains unclear whether the covertly aware vegetative state (VS) constitutes a separate diagnostic category or, damage to the motor system is contributing to reduced responsiveness in the broader PDOC group

Summary

Introduction

The current gold-standard for diagnosing Prolonged Disorders of Consciousness (PDOC) is standardized behavioural scales (e.g., Coma Recovery Scale-Revised (CRS-R); Giacino and Kalmar, 2004), which require the patient to demonstrate their level of awareness through overt responses. Recent studies have demonstrated that behavioural assessments, even by experienced teams, fail to diagnose a small group of VS patients, who show no signs of awareness externally but are able to show them covertly during functional neuroimaging tasks (Boly et al, 2007; Coleman et al, 2009; Fernández-Espejo and Owen, 2013; Owen et al, 2006). These typically involve motor imagery tasks (e.g., the patient is asked to imagine playing tennis; Fernández-Espejo and Owen, 2013; Monti et al, 2010) where the patients' neural responses are used as a proxy for volitional behavioural command-following; an ability that is clinically used as a measure of awareness

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