Enhanced Somatosensory Inhibition Sharpens Hand Representation and Sensorimotor Skills in Pianists

Overview

Journal J Neurosci

Specialty Neurology

Date 2025 Jan 2

PMID 39746821

Authors

Masato Hirano

Yudai Kimoto

Sachiko Shiotani

Shinichi Furuya

Affiliations

Soon will be listed here.

Abstract

Dexterous motor skills, like those needed for playing musical instruments and sports, require the somatosensory system to accurately and rapidly process somatosensory information from multiple body parts. This is challenging due to the convergence of afferent inputs from different body parts into a single neuron and the overlapping representation of neighboring body parts in the somatosensory cortices. How do trained individuals, such as pianists and athletes, manage this? Here, a series of five experiments with pianists and nonmusicians (female and male) shows that pianists have enhanced inhibitory function in the somatosensory system, which isolates the processing of somatosensory afferent inputs from each finger. This inhibitory function was assessed using a paired-pulse paradigm of somatosensory evoked potentials in electroencephalography, which measures the suppressive effect of a first stimulus [i.e., conditioning stimulus (CS)] on the response to a subsequent second stimulus. We found that pianists and nonmusicians showed an inhibitory response to the sequential stimuli to the peripheral somatosensory nerve at the wrist when the CS was intense. However, only pianists exhibited an inhibitory response to a weak CS, indicating enhanced inhibitory function in pianists. Additionally, the CS increased the information content segregating individual fingers represented in the cortical activity evoked by passive finger movements and improved the perception of fast multifinger sequential movements, specifically for pianists. Our findings provide the first evidence for experience-dependent plasticity in somatosensory inhibitory function and highlight its role in the expert motor performance of pianists.

References

Iwamura Y, Tanaka M, Hikosaka O . Overlapping representation of fingers in the somatosensory cortex (area 2) of the conscious monkey. Brain Res. 1980; 197(2):516-20. DOI: 10.1016/0006-8993(80)91139-7. View

Trzcinski N, Hsiao S, Connor C, Gomez-Ramirez M . Multi-finger receptive field properties in primary somatosensory cortex: A revised account of the spatiotemporal integration functions of area 3b. Cell Rep. 2023; 42(3):112176. DOI: 10.1016/j.celrep.2023.112176. View

Altenmuller E, Furuya S . Brain Plasticity and the Concept of Metaplasticity in Skilled Musicians. Adv Exp Med Biol. 2016; 957:197-208. DOI: 10.1007/978-3-319-47313-0_11. View

Ejaz N, Hamada M, Diedrichsen J . Hand use predicts the structure of representations in sensorimotor cortex. Nat Neurosci. 2015; 18(7):1034-40. DOI: 10.1038/nn.4038. View

Elbert T, Pantev C, Wienbruch C, Rockstroh B, Taub E . Increased cortical representation of the fingers of the left hand in string players. Science. 1995; 270(5234):305-7. DOI: 10.1126/science.270.5234.305. View

Seiss E, Hesse C, Drane S, Oostenveld R, Wing A, Praamstra P . Proprioception-related evoked potentials: origin and sensitivity to movement parameters. Neuroimage. 2002; 17(1):461-8. DOI: 10.1006/nimg.2002.1211. View

Ragert P, Becker M, Tegenthoff M, Pleger B, Dinse H . Sustained increase of somatosensory cortex excitability by 5 Hz repetitive transcranial magnetic stimulation studied by paired median nerve stimulation in humans. Neurosci Lett. 2004; 356(2):91-4. DOI: 10.1016/j.neulet.2003.11.034. View

Iwamura Y, Tanaka M, Sakamoto M, Hikosaka O . Rostrocaudal gradients in the neuronal receptive field complexity in the finger region of the alert monkey's postcentral gyrus. Exp Brain Res. 1993; 92(3):360-8. DOI: 10.1007/BF00229023. View

Ogawa K, Mitsui K, Imai F, Nishida S . Long-term training-dependent representation of individual finger movements in the primary motor cortex. Neuroimage. 2019; 202:116051. DOI: 10.1016/j.neuroimage.2019.116051. View

10.

David-Jurgens M, Dinse H . Effects of aging on paired-pulse behavior of rat somatosensory cortical neurons. Cereb Cortex. 2009; 20(5):1208-16. PMC: 2852507. DOI: 10.1093/cercor/bhp185. View

11.

Delorme A, Makeig S . EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods. 2004; 134(1):9-21. DOI: 10.1016/j.jneumeth.2003.10.009. View

12.

Hirano M, Kimoto Y, Furuya S . Specialized Somatosensory-Motor Integration Functions in Musicians. Cereb Cortex. 2019; 30(3):1148-1158. DOI: 10.1093/cercor/bhz154. View

13.

Gandevia S, Burke D, McKeon B . Convergence in the somatosensory pathway between cutaneous afferents from the index and middle fingers in man. Exp Brain Res. 1983; 50(2-3):415-25. DOI: 10.1007/BF00239208. View

14.

Furuya S, Flanders M, Soechting J . Hand kinematics of piano playing. J Neurophysiol. 2011; 106(6):2849-64. PMC: 3234081. DOI: 10.1152/jn.00378.2011. View

15.

Kimoto Y, Oku T, Furuya S . Neuromuscular and biomechanical functions subserving finger dexterity in musicians. Sci Rep. 2019; 9(1):12224. PMC: 6704118. DOI: 10.1038/s41598-019-48718-9. View

16.

Madigan R, Williams D . Maximum-likelihood psychometric procedures in two-alternative forced-choice: evaluation and recommendations. Percept Psychophys. 1987; 42(3):240-9. DOI: 10.3758/bf03203075. View

17.

Sadnicka A, Wiestler T, Butler K, Altenmuller E, Edwards M, Ejaz N . Intact finger representation within primary sensorimotor cortex of musician's dystonia. Brain. 2022; 146(4):1511-1522. PMC: 10115231. DOI: 10.1093/brain/awac356. View

18.

Lang C, Schieber M . Human finger independence: limitations due to passive mechanical coupling versus active neuromuscular control. J Neurophysiol. 2004; 92(5):2802-10. DOI: 10.1152/jn.00480.2004. View

19.

Munte T, Altenmuller E, Jancke L . The musician's brain as a model of neuroplasticity. Nat Rev Neurosci. 2002; 3(6):473-8. DOI: 10.1038/nrn843. View

20.

Ritchie J, Lee Masson H, Bracci S, Op de Beeck H . The unreliable influence of multivariate noise normalization on the reliability of neural dissimilarity. Neuroimage. 2021; 245:118686. DOI: 10.1016/j.neuroimage.2021.118686. View