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      Feasibility of using fNIRS to explore motor-related regional haemodynamic signal changes in patients with sensorimotor impairment and healthy controls: A pilot study

      research-article
      a , b , * , b , a , c , a , c , d , b
      Restorative Neurology and Neuroscience
      IOS Press
      Spinal cord injury, tendon transfer, plasticity, motor cortex, functional near-infrared spectroscopy

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          Abstract

          Background:

          While functional near-infrared spectroscopy (fNIRS) can provide insight into cortical brain activity during motor tasks in healthy and diseased populations, the feasibility of using fNIRS to assess haemoglobin-evoked responses to reanimated upper limb motor function in patients with tetraplegia remains unknown.

          Objective:

          The primary objective of this pilot study is to determine the feasibility of using fNIRS to assess cortical signal intensity changes during upper limb motor tasks in individuals with surgically restored grip functions. The secondary objectives are: 1) to collect pilot data on individuals with tetraplegia to determine any trends in the cortical signal intensity changes as measured by fNIRS and 2) to compare cortical signal intensity changes in affected individuals versus age-appropriate healthy volunteers. Specifically, patients presented with tetraplegia, a type of paralysis resulting from a cervical spinal cord injury causing loss of movement and sensation in both lower and upper limbs. All patients have their grip functions restored by surgical tendon transfer, a procedure which constitutes a unique, focused stimulus for brain plasticity.

          Method:

          fNIRS is used to assess changes in cortical signal intensity during the performance of two motor tasks (isometric elbow and thumb flexion). Six individuals with tetraplegia and six healthy controls participate in the study. A block paradigm is utilized to assess contralateral and ipsilateral haemodynamic responses in the premotor cortex (PMC) and primary motor cortex (M1). We assess the amplitude of the optical signal and spatial features during the paradigms. The accuracy of channel locations is maximized through 3D digitizations of channel locations and co-registering these locations to template atlas brains. A general linear model approach, with short-separation regression, is used to extract haemodynamic response functions at the individual and group levels.

          Results:

          Peak oxyhaemoglobin (oxy-Hb) changes in PMC appear to be particularly bilateral in nature in the tetraplegia group during both pinch and elbow trials whereas for controls, a bilateral PMC response is not especially evident. In M1 / primary sensory cortex (S1), the oxy-Hb responses to the pinch task are mainly contralateral in both groups, while for the elbow flexion task, lateralization is not particularly clear.

          Conclusions:

          This pilot study shows that the experimental setup is feasible for assessing brain activation using fNIRS during volitional upper limb motor tasks in individuals with surgically restored grip functions. Cortical signal changes in brain regions associated with upper extremity sensorimotor processing appear to be larger and more bilateral in nature in the tetraplegia group than in the control group. The bilateral hemispheric response in the tetraplegia group may reflect a signature of adaptive brain plasticity mechanisms. Larger studies than this one are needed to confirm these findings and draw reliable conclusions.

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          Most cited references47

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          HomER: a review of time-series analysis methods for near-infrared spectroscopy of the brain.

          Near-infrared spectroscopy (NIRS) is a noninvasive neuroimaging tool for studying evoked hemodynamic changes within the brain. By this technique, changes in the optical absorption of light are recorded over time and are used to estimate the functionally evoked changes in cerebral oxyhemoglobin and deoxyhemoglobin concentrations that result from local cerebral vascular and oxygen metabolic effects during brain activity. Over the past three decades this technology has continued to grow, and today NIRS studies have found many niche applications in the fields of psychology, physiology, and cerebral pathology. The growing popularity of this technique is in part associated with a lower cost and increased portability of NIRS equipment when compared with other imaging modalities, such as functional magnetic resonance imaging and positron emission tomography. With this increasing number of applications, new techniques for the processing, analysis, and interpretation of NIRS data are continually being developed. We review some of the time-series and functional analysis techniques that are currently used in NIRS studies, we describe the practical implementation of various signal processing techniques for removing physiological, instrumental, and motion-artifact noise from optical data, and we discuss the unique aspects of NIRS analysis in comparison with other brain imaging modalities. These methods are described within the context of the MATLAB-based graphical user interface program, HomER, which we have developed and distributed to facilitate the processing of optical functional brain data.
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            NIRS-SPM: statistical parametric mapping for near-infrared spectroscopy.

            Near infrared spectroscopy (NIRS) is a non-invasive method to measure brain activity via changes in the degree of hemoglobin oxygenation through the intact skull. As optically measured hemoglobin signals strongly correlate with BOLD signals, simultaneous measurement using NIRS and fMRI promises a significant mutual enhancement of temporal and spatial resolutions. Although there exists a powerful statistical parametric mapping tool in fMRI, current public domain statistical tools for NIRS have several limitations related to the quantitative analysis of simultaneous recording studies with fMRI. In this paper, a new public domain statistical toolbox known as NIRS-SPM is described. It enables the quantitative analysis of NIRS signal. More specifically, NIRS data are statistically analyzed based on the general linear model (GLM) and Sun's tube formula. The p-values are calculated as the excursion probability of an inhomogeneous random field on a representation manifold that is dependent on the structure of the error covariance matrix and the interpolating kernels. NIRS-SPM not only enables the calculation of activation maps of oxy-, deoxy-hemoglobin and total hemoglobin, but also allows for the super-resolution localization, which is not possible using conventional analysis tools. Extensive experimental results using finger tapping and memory tasks confirm the viability of the proposed method.
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              The role of ipsilateral premotor cortex in hand movement after stroke.

              Movement of an affected hand after stroke is associated with increased activation of ipsilateral motor cortical areas, suggesting that these motor areas in the undamaged hemisphere may adaptively compensate for damaged or disconnected regions. However, this adaptive compensation has not yet been demonstrated directly. Here we used transcranial magnetic stimulation (TMS) to interfere transiently with processing in the ipsilateral primary motor or dorsal premotor cortex (PMd) during finger movements. TMS had a greater effect on patients than controls in a manner that depended on the site, hemisphere, and time of stimulation. In patients with right hemiparesis (but not in healthy controls), TMS applied to PMd early (100 ms) after the cue to move slowed simple reaction-time finger movements by 12% compared with controls. The relative slowing of movements with ipsilateral PMd stimulation in patients correlated with the degree of motor impairment, suggesting that functional recruitment of ipsilateral motor areas was greatest in the more impaired patients. We also used functional magnetic resonance imaging to monitor brain activity in these subjects as they performed the same movements. Slowing of reaction time after premotor cortex TMS in the patients correlated inversely with the relative hemispheric lateralization of functional magnetic resonance imaging activation in PMd. This inverse correlation suggests that the increased activation in ipsilateral cortical motor areas during movements of a paretic hand, shown in this and previous functional imaging studies, represents a functionally relevant, adaptive response to the associated brain injury.
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                Author and article information

                Journal
                Restor Neurol Neurosci
                Restor Neurol Neurosci
                RNN
                Restorative Neurology and Neuroscience
                IOS Press (Nieuwe Hemweg 6B, 1013 BG Amsterdam, The Netherlands )
                0922-6028
                1878-3627
                08 July 2023
                08 December 2023
                2023
                : 41
                : 3-4
                : 91-101
                Affiliations
                [a ] Center for Advanced Reconstruction of Extremities (C.A.R.E.), Sahlgrenska University Hospital , Mölndal, Sweden
                [b ] Institute of Neuroscience and Physiology, Sahlgrenska Academy, University of Gothenburg , Gothenburg, Sweden
                [c ] Department of Hand Surgery, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg , Gothenburg, Sweden
                [d ] Department of Medical Physics and Biomedical Engineering, Biomedical Optics Research Laboratory, University College London , UK
                Author notes
                [* ]Corresponding author: Lina Bunketorp Käll, Assoc. Prof. C.A.R.E. Sahlgrenska University Hospital/Mölndal House U1, 6th Floor 431 80 Mölndal, Sweden. Tel.: +46 709 723101; E-mail: lina.bunketorp-kall@ 123456neuro.gu.se .
                Article
                RNN221292
                10.3233/RNN-221292
                10741372
                37458052
                c849ab9f-aafa-46c0-b56c-0b1e4a5f7366
                © 2023 – The authors. Published by IOS Press

                This is an open access article distributed under the terms of the Creative Commons Attribution (CC BY 4.0) License.

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                Categories
                Research Report

                spinal cord injury,tendon transfer,plasticity,motor cortex,functional near-infrared spectroscopy

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