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20 Hz Steady-State Response in Somatosensory Cortex During Induction of Tactile Perceptual Learning Through LTP-Like Sensory Stimulation

The induction of synaptic plasticity requires the presence of temporally patterned neural activity. Numerous cellular studies in animals and brain slices have demonstrated that long-term potentiation (LTP) enhances synaptic transmission, which can be evoked by high-frequency intermittent stimulation...

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Autores principales: Brickwedde, Marion, Schmidt, Marie D., Krüger, Marie C., Dinse, Hubert R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7339616/
https://www.ncbi.nlm.nih.gov/pubmed/32694988
http://dx.doi.org/10.3389/fnhum.2020.00257
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author Brickwedde, Marion
Schmidt, Marie D.
Krüger, Marie C.
Dinse, Hubert R.
author_facet Brickwedde, Marion
Schmidt, Marie D.
Krüger, Marie C.
Dinse, Hubert R.
author_sort Brickwedde, Marion
collection PubMed
description The induction of synaptic plasticity requires the presence of temporally patterned neural activity. Numerous cellular studies in animals and brain slices have demonstrated that long-term potentiation (LTP) enhances synaptic transmission, which can be evoked by high-frequency intermittent stimulation. In humans, plasticity processes underlying perceptual learning can be reliably induced by repetitive, LTP-like sensory stimulation. These protocols lead to improvement of perceptual abilities parallel to widespread remodeling of cortical processing. However, whether maintained rhythmic cortical activation induced by the LTP-like stimulation is also present during human perceptual learning experiments, remains elusive. To address this question, we here applied a 20 Hz intermittent stimulation protocol for 40 min to the index-, middle- and ring-fingers of the right hand, while continuously recording EEG over the hand representation in primary somatosensory cortex in young adult participants. We find that each train of stimulation initiates a transient series of sensory-evoked potentials which accumulate after about 500 ms into a 20 Hz steady-state response persisting over the entire period of the 2-s-train. During the inter-train interval, no consistent evoked activity can be detected. This response behavior is maintained over the whole 40 min of stimulation without any indication of habituation. However, the early stimulation evoked potentials (SEPs) and the event-related desynchronization (ERD) during the steady-state response change over the 40 min of stimulation. In a second experiment, we demonstrate in a separate cohort of participants that the here-applied pneumatic type of stimulation results in improvement of tactile acuity as typically observed for electrically applied 20 Hz intermittent stimulation. Our data demonstrate that repetitive stimulation using a 20 Hz protocol drives rhythmic activation in the hand representation of somatosensory cortex, which is sustained during the entire stimulation period. At the same time, cortical excitability increases as indicated by altered ERD and SEP amplitudes. Our results, together with previous data underlining the dependence of repetitive sensory stimulation effects on NMDA-receptor activation, support the view that repetitive sensory stimulation elicits LTP-like processes in the cortex, thereby facilitating perceptual learning processes.
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spelling pubmed-73396162020-07-20 20 Hz Steady-State Response in Somatosensory Cortex During Induction of Tactile Perceptual Learning Through LTP-Like Sensory Stimulation Brickwedde, Marion Schmidt, Marie D. Krüger, Marie C. Dinse, Hubert R. Front Hum Neurosci Neuroscience The induction of synaptic plasticity requires the presence of temporally patterned neural activity. Numerous cellular studies in animals and brain slices have demonstrated that long-term potentiation (LTP) enhances synaptic transmission, which can be evoked by high-frequency intermittent stimulation. In humans, plasticity processes underlying perceptual learning can be reliably induced by repetitive, LTP-like sensory stimulation. These protocols lead to improvement of perceptual abilities parallel to widespread remodeling of cortical processing. However, whether maintained rhythmic cortical activation induced by the LTP-like stimulation is also present during human perceptual learning experiments, remains elusive. To address this question, we here applied a 20 Hz intermittent stimulation protocol for 40 min to the index-, middle- and ring-fingers of the right hand, while continuously recording EEG over the hand representation in primary somatosensory cortex in young adult participants. We find that each train of stimulation initiates a transient series of sensory-evoked potentials which accumulate after about 500 ms into a 20 Hz steady-state response persisting over the entire period of the 2-s-train. During the inter-train interval, no consistent evoked activity can be detected. This response behavior is maintained over the whole 40 min of stimulation without any indication of habituation. However, the early stimulation evoked potentials (SEPs) and the event-related desynchronization (ERD) during the steady-state response change over the 40 min of stimulation. In a second experiment, we demonstrate in a separate cohort of participants that the here-applied pneumatic type of stimulation results in improvement of tactile acuity as typically observed for electrically applied 20 Hz intermittent stimulation. Our data demonstrate that repetitive stimulation using a 20 Hz protocol drives rhythmic activation in the hand representation of somatosensory cortex, which is sustained during the entire stimulation period. At the same time, cortical excitability increases as indicated by altered ERD and SEP amplitudes. Our results, together with previous data underlining the dependence of repetitive sensory stimulation effects on NMDA-receptor activation, support the view that repetitive sensory stimulation elicits LTP-like processes in the cortex, thereby facilitating perceptual learning processes. Frontiers Media S.A. 2020-06-30 /pmc/articles/PMC7339616/ /pubmed/32694988 http://dx.doi.org/10.3389/fnhum.2020.00257 Text en Copyright © 2020 Brickwedde, Schmidt, Krüger and Dinse. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Brickwedde, Marion
Schmidt, Marie D.
Krüger, Marie C.
Dinse, Hubert R.
20 Hz Steady-State Response in Somatosensory Cortex During Induction of Tactile Perceptual Learning Through LTP-Like Sensory Stimulation
title 20 Hz Steady-State Response in Somatosensory Cortex During Induction of Tactile Perceptual Learning Through LTP-Like Sensory Stimulation
title_full 20 Hz Steady-State Response in Somatosensory Cortex During Induction of Tactile Perceptual Learning Through LTP-Like Sensory Stimulation
title_fullStr 20 Hz Steady-State Response in Somatosensory Cortex During Induction of Tactile Perceptual Learning Through LTP-Like Sensory Stimulation
title_full_unstemmed 20 Hz Steady-State Response in Somatosensory Cortex During Induction of Tactile Perceptual Learning Through LTP-Like Sensory Stimulation
title_short 20 Hz Steady-State Response in Somatosensory Cortex During Induction of Tactile Perceptual Learning Through LTP-Like Sensory Stimulation
title_sort 20 hz steady-state response in somatosensory cortex during induction of tactile perceptual learning through ltp-like sensory stimulation
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7339616/
https://www.ncbi.nlm.nih.gov/pubmed/32694988
http://dx.doi.org/10.3389/fnhum.2020.00257
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