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. 2023 Feb;27(2):257-277.
doi: 10.1002/ejp.2057. Epub 2022 Dec 1.

Extensive sensorimotor training enhances nociceptive cortical responses in healthy individuals

Anna M Zamorano  1 , Boris Kleber  2 , Federico Arguissain  1 , Peter Vuust  2 , Herta Flor  1   3 , Thomas Graven-Nielsen  1
Affiliations

Extensive sensorimotor training enhances nociceptive cortical responses in healthy individuals

Anna M Zamorano et al. Eur J Pain. 2023 Feb.

Abstract

Background: Prolonged and repeated sensorimotor training is a crucial driver for promoting use-dependent plasticity, but also a main risk factor for developing musculoskeletal pain syndromes, yet the neural underpinnings that link repetitive movements to abnormal pain processing are unknown.

Methods: Twenty healthy musicians, one of the best in vivo models to study use-dependent plasticity, and 20 healthy non-musicians were recruited. Perceptual thresholds, reaction times (RTs) and event-related potentials (ERPs) were recorded using nociceptive intra-epidermal and non-nociceptive transcutaneous electrical stimulation.

Results: In response to comparable stimulus intensities, musicians compared to non-musicians showed larger non-nociceptive N140 (associated with higher activation of regions within the salience network), higher nociceptive N200 ERPs (associated with higher activation of regions within the sensorimotor network) and faster RTs to both stimuli. Non-musicians showed larger non-nociceptive P200 ERP. Notably, a similar P200 component prominently emerged during nociceptive stimulation in non-musicians. Across participants, larger N140 and N200 ERPs were associated with RTs, whereas the amount of daily practice in musicians explained non-nociceptive P200 and nociceptive P300 ERPs.

Conclusions: These novel findings indicate that the mechanisms by which extensive sensorimotor training promotes use-dependent plasticity in multisensory neural structures may also shape the neural signatures of nociceptive processing in healthy individuals.

Significance: Repetitive sensorimotor training may increase the responsiveness of nociceptive evoked potentials. These novel data highlight the importance of repetitive sensorimotor practice as a contributing factor to the interindividual variability of nociceptive-related potentials.

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Conflict of interest statement

None.

Figures

FIGURE 1
FIGURE 1
Brain responses and topographies of nociceptive stimuli. (a) Grand‐averaged event‐related potentials elicited by the nociceptive electrical stimulation at the hand and illustrated at nine topographical regions of interest (ROIs; bottom center) in musicians (red lines) and non‐musicians (blue lines). ROIs: frontocentral (FC), central (C) and centroparietal (CP). Marked time periods windows in grey indicate time periods and ROIs with significant differences between musicians and non‐musicians (p < 0.05). Negative is plotted downward. Amplitudes across all ROIs indicate larger N200 and smaller P100 and P200 components. (b) Amplitude scalp topography of each nociceptive component in musicians and non‐musicians. Scalp topographies shown are generated at 100 ms (P100), 180 ms (N200), 200 ms (P200), and 360 ms (P300).
FIGURE 2
FIGURE 2
Brain responses and topographies of non‐nociceptive somatosensory stimuli. (a) Grand‐averaged event‐related potentials elicited by the non‐nociceptive electrical stimulation at the hand and illustrated at nine topographical regions of interest (ROIs; bottom centre) in musicians (red lines) and non‐musicians (blue lines). ROIs: frontocentral (FC), central (C) and centroparietal (CP). Marked time periods windows in grey indicate time periods and ROIs in which there were significant differences between musicians and non‐musicians (p < 0.05). Negative is plotted downward. Amplitudes across all ROIs were larger for the N140 and smaller for the P100 and P200 components in musicians compared to non‐musicians. (b) Amplitude scalp topography of each non‐nociceptive component in musicians and non‐musicians. Scalp topographies shown are generated at 45 ms (P50), 100 ms (P100), 140 ms (N140), 200 ms (P200) and 300 ms (P300).
FIGURE 3
FIGURE 3
Source localization maps in response to nociceptive electrical stimulation in musicians (top) and non‐musicians (bottom). Source maps shown are generated at 180 ms (N200), 200 ms (P200) and 350 ms (P300).
FIGURE 4
FIGURE 4
Contrast maps of whole‐brain activity between musicians and non‐musicians (red lines at N200 in response to nociceptive electrical stimulation. Significance thresholds were set at p < 0.05, and multiple comparisons were false discovery rate (FDR) corrected. Waveforms correspond to the entire time courses of the neural sources in musicians (black lines) and non‐musicians (red‐lines) at the left primary somatosensory cortex (SI, a), the left MI and paracentral lobule (MI/PCL, b), the left supplementary motor area (SMA, c) and the left posterior cingulate cortex (PCC, d).
FIGURE 5
FIGURE 5
Source localization maps in response to non‐nociceptive electrical stimulation in musicians (top) and non‐musicians (bottom). Source maps shown are generated at 140 ms (N140), 200 ms (P200) and 300 ms (P300).
FIGURE 6
FIGURE 6
Contrast maps of whole‐brain activity between musicians and non‐musicians at N140 in response to non‐nociceptive electrical stimulation. Significance thresholds were set at p < 0.05, and multiple comparisons were false discovery rate (FDR) corrected. Waveforms correspond to the entire time courses of the neural sources in musicians (black lines) and nonmusicians (red lines) at the right angular gyrus (AG, a), the right superior parietal lobule (SPL, b), the right temporal pole (TP, c), the right orbitofrontal cortex (OFC, d), the left posterior cingulate cortex (PCC, e), the right anterior insula (f), right supplementary motor area (SMA, g) and the right precuneus (h).
FIGURE 7
FIGURE 7
Significant correlations of event‐related potentials, reaction times and daily practice. (a) The non‐nociceptive N140 (left) and nociceptive N200 (right) peak amplitudes correlate with their respective non‐nociceptive and nociceptive electrical stimulation reaction times. Musicians are represented by black dots and non‐musicians by grey dots. (b) In musicians, the amount of daily practice (h) correlates with the peak amplitudes of the non‐nociceptive P200 and the nociceptive P300 components. Fit lines indicate correlations between respective variables.
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