Resting State EEG Directed Functional Connectivity Unveils Changes in Motor Network Organization in Subacute Stroke Patients After Rehabilitation

Abstract

Brain plasticity and functional reorganization are mechanisms behind functional motor recovery of patients after an ischemic stroke. The study of resting-state motor network functional connectivity by means of EEG proved to be useful in investigating changes occurring in the information flow and find correlation with motor function recovery. In the literature, most studies applying EEG to post-stroke patients investigated the undirected functional connectivity of interacting brain regions. Quite recently, works started to investigate the directionality of the connections and many approaches or features have been proposed, each of them being more suitable to describe different aspects, e.g., direct or indirect information flow between network nodes, the coupling strength or its characteristic oscillation frequency. Each work chose one specific measure, despite in literature there is not an agreed consensus, and the selection of the most appropriate measure is still an open issue. In an attempt to shed light on this methodological aspect, we propose here to combine the information of direct and indirect coupling provided by two frequency-domain measures based on Granger’s causality, i.e., the directed coherence (DC) and the generalized partial directed coherence (gPDC), to investigate the longitudinal changes of resting-state directed connectivity associated with sensorimotor rhythms α and β, occurring in 18 sub-acute ischemic stroke patients who followed a rehabilitation treatment. Our results showed a relevant role of the information flow through the pre-motor regions in the reorganization of the motor network after the rehabilitation in the sub-acute stage. In particular, DC highlighted an increase in intra-hemispheric coupling strength between pre-motor and primary motor areas, especially in ipsi-lesional hemisphere in both α and β frequency bands, whereas gPDC was more sensitive in the detection of those connection whose variation was mostly represented within the population. A decreased causal flow from contra-lesional premotor cortex towards supplementary motor area was detected in both α and β frequency bands and a significant reinforced inter-hemispheric connection from ipsi to contra-lesional pre-motor cortex was observed in β frequency. Interestingly, the connection from contra towards ipsilesional pre-motor area correlated with upper limb motor recovery in α band. The usage of two different measures of directed connectivity allowed a better comprehension of those coupling changes between brain motor regions, either direct or mediated, which mostly were influenced by the rehabilitation, revealing a particular involvement of the pre-motor areas in the cerebral functional reorganization.

A Narrative Review on Multi-Domain Instrumental Approaches to Evaluate Neuromotor Function in Rehabilitation

“…Indeed, brain network reorganization has been demonstrated to depend on time after stroke [ 84 ], and an increase in inter-hemispheric connectivity, particularly between the primary motor cortexes in alpha and beta frequencies, was found to positively correlate with motor outcome improvement [ 71 , 82 , 83 ]. Conversely, an increase in RS-directed connectivity measures, from pre-motor towards primary motor intra-hemispheric regions, was found in sub-acute patients assessed before and after rehabilitation treatment [ 85 ]. Hoshino et al in 2021 found higher intra-hemispheric FC in both hemispheres in RS and during ankle movement [ 71 ].…”

Connectivity Analysis in EEG Data: A Tutorial Review of the State of the Art and Emerging Trends

“…The normalized DTF was used for assessing directed functional connectivity from EEG recordings in one subject who received a new prosthodontic provisional implant as a substitute for previous dental repairs [ 169 ]. DC and gPDC were exploited to investigate the changes in resting-state directed connectivity associated with sensorimotor rhythms and , occurring in stroke patients who followed a rehabilitation treatment [ 170 ]. The results suggest that using different methods to measure directed connectivity can improve the understanding of how brain motor regions are connected between each other.…”

The role of neurophysiological tools in the evaluation of ischemic stroke evolution: a narrative review

“…Finally, EEG connectivity appears to be locally impaired in chronic stroke, with significant modifications in connectivity from the subacute to the chronic stage ( 83 ). In the chronic phase, the reduction of the beta band (12.5–30.0 Hz) oscillatory activity in the motor cortex is an index of motor impairment ( 84 ).…”