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      Prismatic Adaptation Modulates Oscillatory EEG Correlates of Motor Preparation but Not Visual Attention in Healthy Participants

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          Abstract

          Prismatic adaption (PA) has been proposed as a tool to induce neural plasticity and is used to help neglect rehabilitation. It leads to a recalibration of visuomotor coordination during pointing as well as to aftereffects on a number of sensorimotor and attention tasks, but whether these effects originate at a motor or attentional level remains a matter of debate. Our aim was to further characterize PA aftereffects by using an approach that allows distinguishing between effects on attentional and motor processes. We recorded EEG in healthy human participants (9 females and 7 males) while performing a new double step, anticipatory attention/motor preparation paradigm before and after adaptation to rightward-shifting prisms, with neutral lenses as a control. We then examined PA aftereffects through changes in known oscillatory EEG signatures of spatial attention orienting and motor preparation in the alpha and beta frequency bands. Our results were twofold. First, we found PA to rightward-shifting prisms to selectively affect EEG signatures of motor but not attentional processes. More specifically, PA modulated preparatory motor EEG activity over central electrodes in the right hemisphere, contralateral to the PA-induced, compensatory leftward shift in pointing movements. No effects were found on EEG signatures of spatial attention orienting over occipitoparietal sites. Second, we found the PA effect on preparatory motor EEG activity to dominate in the beta frequency band. We conclude that changes to intentional visuomotor, rather than attentional visuospatial, processes underlie the PA aftereffect of rightward-deviating prisms in healthy participants.

          SIGNIFICANCE STATEMENT Prismatic adaptation (PA) has been proposed as a tool to induce neural plasticity in both healthy participants and patients, due to its aftereffect impacting on a number of visuospatial and visuomotor functions. However, the neural mechanisms underlying PA aftereffects are poorly understood as only little neuroimaging evidence is available. Here, we examined, for the first time, the origin of PA aftereffects studying oscillatory brain activity. Our results show a selective modulation of preparatory motor activity following PA in healthy participants but no effect on attention-related activity. This provides novel insight into the PA aftereffect in the healthy brain and may help to inform interventions in neglect patients.

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          Most cited references64

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          The Role of Alpha-Band Brain Oscillations as a Sensory Suppression Mechanism during Selective Attention

          Evidence has amassed from both animal intracranial recordings and human electrophysiology that neural oscillatory mechanisms play a critical role in a number of cognitive functions such as learning, memory, feature binding and sensory gating. The wide availability of high-density electrical and magnetic recordings (64–256 channels) over the past two decades has allowed for renewed efforts in the characterization and localization of these rhythms. A variety of cognitive effects that are associated with specific brain oscillations have been reported, which range in spectral, temporal, and spatial characteristics depending on the context. Our laboratory has focused on investigating the role of alpha-band oscillatory activity (8–14 Hz) as a potential attentional suppression mechanism, and this particular oscillatory attention mechanism will be the focus of the current review. We discuss findings in the context of intersensory selective attention as well as intrasensory spatial and feature-based attention in the visual, auditory, and tactile domains. The weight of evidence suggests that alpha-band oscillations can be actively invoked within cortical regions across multiple sensory systems, particularly when these regions are involved in processing irrelevant or distracting information. That is, a central role for alpha seems to be as an attentional suppression mechanism when objects or features need to be specifically ignored or selected against.
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            Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization.

            Human scalp EEG studies have shown that event-related desynchronization (ERD) in the alpha (8-13 Hz) and beta (15-25 Hz) bands may be used to detect functional activation of sensorimotor cortex. However, in most previous studies somatotopy has not been examined in detail and brief, self-paced movements, focusing on the planning of motor output, have been used. We recorded electrocorticographic (ECoG) signals in five clinical subjects during a visual-motor decision task that was designed to activate the representations of different body parts in sensorimotor cortex. To focus more on execution of motor output than on its planning, subjects were instructed to make sustained isometric muscle contractions in different body parts (tongue protrusion, fist-clenching or foot dorsiflexion) in response to randomized visual stimuli depicting each action. ECoG spectral analysis utilized a mixed-effects analysis of variance model in which within-trial temporal dependencies were taken into account, and the magnitude and statistical significance of alpha and beta ERDs were mapped onto a surface rendering of each subject's brain MRI. Cortical electrical stimulation was performed in all subjects for clinical purposes, and the resulting maps of sensorimotor function were compared with those generated by ECoG spectral analysis. During the early phases of the motor responses, alpha ERD commonly occurred in a diffuse spatial pattern that was not somatotopically specific. During the late phases, the spatial pattern of alpha ERD usually became more focused and somatotopically specific. Maps of alpha ERD were closer to cortical stimulation maps when alpha ERD was sustained throughout the late phases of the motor responses. Thus, the topography of alpha ERD more resembled traditional somatotopy when its temporal profile approximated that of the motor response. The topography of beta ERD was often more discrete and somatotopically specific than that of alpha ERD, but beta ERD was often transient and sometimes absent. Sometimes, unilateral limb movement produced sustained alpha and beta ERD over bilateral sensorimotor cortices, with overlapping patterns for different body parts. The topographical spread of alpha ERD beyond expected functional-anatomical boundaries during early (and sometimes late) phases of motor responses invites a re-examination of traditional assumptions about sensorimotor functional neuroanatomy, as well as the role of alpha ERD as an index of cortical activation. We agree with others that the somatotopic representations of different body parts overlap more than previously thought. Also, unilateral limb movements may be associated with both contralateral and ipsilateral activation of sensorimotor cortex. We conjecture that alpha ERD may reflect activity within a broad synaptic network with distributed cortical representations.
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              Prism adaptation to a rightward optical deviation rehabilitates left hemispatial neglect.

              A large proportion of right-hemisphere stroke patients show hemispatial neglect-a neurological deficit of perception, attention, representation, and/or performing actions within their left-sided space, inducing many functional debilitating effects on everyday life, and responsible for poor functional recovery and ability to benefit from treatment. The frequent parietal locus of the lesion producing neglect reflects the impairment of coordinate transformation used by the nervous system to represent extrapersonal space. Given that adaptation to a visual distortion can provide an efficient way to stimulate neural structures responsible for the transformation of sensorimotor coordinates, the aim of our study was to investigate the effect of prism adaptation on various neglect symptoms, including the pathological shift of the subjective midline to the right. All patients exposed to the optical shift of the visual field to the right were improved on their manual body-midline demonstration and on classical neuropsychological tests. Unlike other physiological manipulations used to improve neglect, this improvement lasted for at least two hours after prism removal and thus could be useful in rehabilitation programmes. The positive effect found for both sensorimotor and more cognitive spatial functions suggests that they share or depend on a common level of space representation linked to multisensory integration.
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                Author and article information

                Journal
                J Neurosci
                J. Neurosci
                jneuro
                jneurosci
                J. Neurosci
                The Journal of Neuroscience
                Society for Neuroscience
                0270-6474
                1529-2401
                31 January 2018
                31 January 2018
                : 38
                : 5
                : 1189-1201
                Affiliations
                [1] 1Dipartimento di Scienze Psicologiche, Pedagogiche e della Formazione, Università degli Studi di Palermo, Palermo 90128, Italy,
                [2] 2Dipartimento NEUROFARBA, Università degli Studi di Firenze, Firenze 50139, Italy,
                [3] 3NeuroTeam Life and Science, Palermo 90143, Italy, and
                [4] 4Centre for Cognitive Neuroimaging, Institute of Neuroscience and Psychology, University of Glasgow, Glasgow G12 8QB, United Kingdom
                Author notes
                Correspondence should be addressed to either of the following: Dr. Gregor Thut, University of Glasgow, 58 Hillhead Street, Glasgow G12 8QB, United Kingdom. Gregor.Thut@ 123456glasgow.ac.uk ; or Dr. Martina Bracco, University of Palermo, Viale delle Scienze, Edificio 15, 90128 Palermo, Italy. martina.bracco@ 123456unifi.it

                Author contributions: M.B., D.V., M.O., and G.T. designed research; M.B. and D.V. performed research; M.B. and D.V. analyzed data; M.B., D.V., M.O., and G.T. wrote the paper.

                *M.B. and D.V. contributed equally to this study.

                Author information
                http://orcid.org/0000-0003-1313-4262
                Article
                1422-17
                10.1523/JNEUROSCI.1422-17.2017
                5792477
                29255004
                ce7c4b5a-5339-476e-90a5-91a76459d77b
                Copyright © 2018 Bracco, Veniero et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 23 May 2017
                : 24 October 2017
                : 14 November 2017
                Categories
                Research Articles
                Behavioral/Cognitive

                aftereffects,attention orienting,brain oscillations,eeg,motor preparation,prismatic adaptation

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