Recovery of sleep EEG patterns in minimally conscious state

Late and progressive alterations of sleep dynamics following central thalamic deep brain stimulation (CT-DBS) in chronic minimally conscious state

Zoe M. Adams, Peter B. Forgacs, Mary M. Conte, Tanya J. Nauvel, Jonathan D. Drover and Nicholas D. Schiff

Clinical Neurophysiology. doi: 10.1016/jclinph 2016.06.028 (2016)

Introduction

We report changes in sleep dynamics recorded in the electroencephalogram (EEG) from a 44 year-old male patient subject (PS) in association with central thalamic deep brain stimulation (CT-DBS). The PS had a long-standing history of severe traumatic brain injury (TBI) occurring at the age of 17 and has remained in a minimally conscious state (MCS) since the time of injury. CT-DBS began 21 years after injury, and sleep EEG measurements were obtained prior to implantation and followed longitudinally over three and a half years post-implantation.

The possible significance of the presence or absence of specific sleep elements as well as their evolution over time is not well characterized in minimally conscious state patients. Patients in MCS exhibit intermittent evidence of responsiveness without the ability to communicate due to lack of consistent or goal-directed movements to external stimuli (Giacino et al. 2002). Compared to patients in the vegetative state (VS), many MCS patients have hallmark features of sleep, such as spindles and slow waves (Landsness et al. 2011). However, these elements are often indistinct and challenging to identify according to the normal criteria for sleep staging in persons without brain injury (Cologan et al. 2010). Rare examples of late recovery have revealed the potential for cognitive capacity in some patients (Voss et al. 2006). Thus, the examination of longitudinal fluctuations in sleep electrophysiology may provide insight into otherwise unmeasured changes in overall brain function.

The examination of sleep in the setting of CT-DBS is warranted because two key elements of healthy sleep—spindles and slow waves—are generated via thalamocortical feedback loops that prominently involve the neurons within the central thalamus (Contreras et al. 1997; David et al. 2013). CT-DBS has been proposed as a method to drive frontostriatal activity in the underactive, widely deafferented brain to facilitate behavioral recovery (Schiff et al. 2007). After severe structural brain injuries such as the one observed in our PS, widespread deafferentation can be expected to produce broad disfacilitation of large-scale cerebral networks (Gold and Lauritzen 2002). The central thalamus has been proposed to play a key role in the maintenance of synaptic activity across the frontostriatal systems during wakeful states following severe brain injuries (Schiff, N.D., 2012; 2010). In support of this hypothesis, CT-DBS produced behavioral improvements in one minimally conscious patient six years after injury (Schiff et al. 2007). Additionally, cortical evoked responses in this patient provided direct evidence of CT-DBS activation of fronto-central cortical regions (Schiff et al. 2007). While our PS did not show overt behavioral improvements as a result of CT-DBS, the changes in sleep dynamics observed from pre- to post-CT-DBS implantation provide insight into electrophysiological consequences of CT-DBS treatment.


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