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Impairments of cortico-cortical connectivity in fine tactile sensation after stroke
Journal of NeuroEngineering and Rehabilitation volume 18, Article number: 34 (2021)
Abstract
Background
Fine tactile sensation plays an important role in motor relearning after stroke. However, little is known about its dynamics in post-stroke recovery, principally due to a lack of effective evaluation on neural responses to fine tactile stimulation. This study investigated the post-stroke alteration of cortical connectivity and its functional structure in response to fine tactile stimulation via textile fabrics by electroencephalogram (EEG)-derived functional connectivity and graph theory analyses.
Method
Whole brain EEG was recorded from 64 scalp channels in 8 participants with chronic stroke and 8 unimpaired controls before and during the skin of the unilateral forearm contacted with a piece of cotton fabric. Functional connectivity (FC) was then estimated using EEG coherence. The fabric stimulation induced FC (SFC) was analyzed by a cluster-based permutation test for the FC in baseline and fabric stimulation. The functional structure of connectivity alteration in the brain was also investigated by assessing the multiscale topological properties of functional brain networks according to the graph theory.
Results
In the SFC distribution, an altered hemispheric lateralization (HL) (HL degree, 14%) was observed when stimulating the affected forearm in the stroke group, compared to stimulation of the unaffected forearm of the stroke group (HL degree, 53%) and those of the control group (HL degrees, 92% for the left and 69% for the dominant right limb). The involvement of additional brain regions, i.e., the distributed attention networks, was also observed when stimulating either limb of the stroke group compared with those of the control. Significantly increased (P < 0.05) global and local efficiencies were found when stimulating the affected forearm compared to the unaffected forearm. A significantly increased (P < 0.05) degree of inter-hemisphere FC (interdegree) mainly within ipsilesional somatosensory region and a significantly diminished degree of intra-hemisphere FC (intradegree) (P < 0.05) in ipsilesional primary somatosensory region were observed when stimulating the affected forearm, compared with the unaffected forearm.
Conclusions
The alteration of cortical connectivity in fine tactile sensation post-stroke was characterized by the compensation from the contralesional hemisphere and distributed attention networks related to involuntary attention. The interhemispheric connectivity could implement the compensation from the contralateral hemisphere to the ipsilesional somatosensory region. Stroke participants also exerted increased cortical activities in fine tactile sensation.
Background
Fine tactile sensation plays an important role in motor relearning after stroke, and participates not only in initiating effective motor behaviors but also in fine-tuning subsequent movements for fine motor control [1,2,3]. It is notable however, that there is a relatively marginal amount of knowledge regarding its dynamics in the process of post-stroke rehabilitation. This is mainly due to a lack of effective evaluation on neural responses to fine tactile stimulation. On the one hand, the traditional measures of fine tactile impairments in clinical practice are disadvantageous in terms of reliability and repeatability without direct cortical detection [3]. For example, the two-point discrimination test depends not only on the pressure applied to the finger by the examiner to induce tactile stimulation, but also on the cognitive and discriminative levels of patients in terms of subtle differences due to the inherently subjective nature of tactile sensation [3]. On the other hand, functional neuroplasticity widely occurs in multiple brain regions, including local and remote areas with respect to the lesion site reorganized after a stroke. This would further result in the cortical reorganization and connectivity disturbance, as previously reported in studies on motor functions [4, 5]. A redistributed pattern from the ipsilesional hemisphere to the contralesional hemisphere is commonly observed during motor or cognitive tasks in stroke participants [6, 7]. However, compared to the extensively studied motor impairments, little is known about the neuroplasticity associated with sensory impairments post-stroke. This is principally due to a lack of evidence regarding the strategies of cortical recruitment particularly in the area of fine tactile sensation.
There are some studies on resting-state functional magnetic resonance imaging (rsfMRI) which examined the changes of cortical recruitment in relation to the tactile impairment post-stroke, as revealed by functional connectivity (FC) [8, 9]. For example, Bannister et al. exploited rsfMRI to examine the relationship between the recovery of tactile sensation and the resting-state FC following a stroke. The results indicated that the changes of resting-state FC between somatosensory regions and distributed regions, including vision and attention networks, were associated with improved tactile sensation within the first 6 months post-stroke [8]. Goodin et al. also used rsfMRI to investigate the effect of different lesion sites in the hemispheres on the functional connectivity of tactile sensation in stroke participants [9]. It was found that the patients with lesions in the right hemisphere had greater intra-hemispheric connectivity from the ipsilesional primary somatosensory cortex (S1) to inferior parietal regions than those with left lesions and unimpaired controls. However, these studies revealed only the alterations of static cortical networks during the resting-state after stroke. Furthermore, fMRI is limited in terms of temporal resolution, despite the advantages of higher spatial resolution and deeper imaging of brain activities beyond the cortical level than electroencephalogram (EEG). In this sense, the fMRI is inadequate when seeking the detection of the cortical activities in transient tactile stimulation, since the sensory neurons change their levels of sensitivity to a constant stimulus over time, i.e., sensory adaptation [10]. Thus, the available results on tactile impairments post-stroke might not be suitable to reveal the strategies of the alteration in cortical connectivity during the tactile sensation, which is a typically transient process [11].
In comparison to fMRI, when evaluating the cortical connectivity, EEG offers a higher degree of temporal resolution when seeking to capture neural activities during transient tasks [12, 13]. In this regard, the EEG-derived FC [14, 15], demonstrating the interaction of information among cortical regions, has been proven to be effective in capturing the alteration of cortical connectivity in transient motor tasks in stroke survivors [16, 17]. For instance, Strens et al. compared the EEG-derived FC during a 25% maximal handgrip task in chronic stroke participants and unimpaired persons [16]. The results revealed greater FC between the ipsilesional supplementary motor area (SMA) and sensorimotor area in the stroke than the unimpaired controls, which might have a dynamically compensatory effect for brain lesion after a stroke. The EEG-derived FC has also been applied to measure the post-stroke alteration in cortical connectivity during the repeated finger extensions with a frequency of 1 Hz. It was found that the intensity of FC between contralesional motor/premotor cortex and SMA was increased in stroke subjects compared with the unimpaired controls [17]. Despite the successful evaluations of the EEG-derived FC for motor neuroplasticity following stroke, its investigation on sensory neuroplasticity has not been well carried out. Such an investigation would have the potential to further develop current understandings of the alteration in cortical connectivity in relation to the tactile impairments post-stroke.
The alteration of cortical connectivity in its functional structure can be visualized by the graph theory-based approach from a network perspective [18, 19], where the EEG channels at different cortical locations and their FCs are topographically represented as nodes and links among them [20]. The graph theory analysis has been adopted to reveal the stroke-induced changes in functional brain networks from local (e.g., single-node connectivity) to global level (e.g., connectivity of the entire brain) represented by indices at difference scales [21]. Thus the examination of the dynamic information processing and neural communication during motor or cognitive tasks was facilitated [22]. De Vico Fallani et al. also examined the functional brain organization in stroke subjects whilst engaging in the finger tapping, where inefficient brain networks were found in stroke participants with a lower capacity to integrate the information from remote brain regions and a lower capacity of processing information in local brain regions, compared with unimpaired persons [21]. Additionally, in a study by Philips et al. on persons with chronic stroke [23], the reduction of graph theoretical indices represented by the parameters of global efficiency, local efficiency and the density of intrahemispheric FC on the unaffected hemisphere was found to correlate with post-stroke motor improvements measured by the increments in the upper-extremity portion of the Fugl-Meyer Assessment (FMUE) after a physical treatment for 12 weeks. However, little has been done using the graph theoretical analysis to understand the functional structure in relation to the connectivity alteration in the brain following the post-stroke tactile impairments.
The purpose of this study was to investigate the post-stroke alteration of cortical connectivity in response to fine tactile stimulation via the textile fabric by EEG-derived functional connectivity analysis. Whole brain EEG was recorded from 64 scalp channels in 8 persons with chronic stroke and 8 age-matched unimpaired controls before and during the unilateral forearm skin contact with cotton fabric. Functional connectivity was then estimated using the EEG coherence method [24]. The fabric stimulation induced functional connectivity (SFC) was analyzed by means of a cluster-based permutation test based on the estimated FC [25]. Furthermore, the multiscale topological properties of functional brain networks were assessed using the graph theory-based method to reveal the functional structure of the connectivity alteration in the brain during transient fine tactile sensation after stroke on multiple levels. Finally, the alteration of brain connectivity in relation to the tactile impairments post-stroke was discussed in detail.
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