Abstract
We tested the hypothesis that the inability to move a pen accurately in a graphic task is partly due to a decrease of afferent somatosensory information resulting from overpressure on the tactile receptors of the fingers holding the pen. To disentangle the depressed somatosensory origin from an altered motor command, we compared a condition in which the participant actively produces pressure on the pen (active grip) with a condition in which pressure is passively applied (passive grip, no grip-related motor command). We expected that the response of the somatosensory cortex to electric stimulation of the wrist’s tactile nerve (i.e., SEP) would be greater in the natural pen grip (baseline condition) than in the two overpressure conditions (actively or passively induced). Fifteen adults were required to trace a geometrical shape in the three grip conditions. The SEP amplitude was not significantly different between the baseline and both overpressure conditions. However, behavioral results showed that drawing accuracy is impaired when the pressure on the pen is increased (passively or actively). Cortical source analyses revealed that the activity of the superior parietal areas (SPL) increased in both overpressure conditions. Our findings suggest that the SPL is critical for sensorimotor integration, by maintaining an internal representation of pen holding. These cortical changes might witness the impaired updating of the finger–pen interaction force for such drawing actions under visual guidance.
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References
Barany DA, Dell-Maggiore V, Viswanathan S, Cieslak M, Grafton ST (2014) Feature interactions enable decoding of sensorimotor transformations for goal-directed movement. J Neurosci 34:6860–6873. https://doi.org/10.1523/JNEUROSCI.5173-13.2014
Blakemore SJ, Wolpert DM, Frith CD (1998) Central cancellation of self-produced tickle sensation. Nat Neurosci 1:635–640. https://doi.org/10.1038/2870
Cavada C, Goldman-Rakic PS (1989) Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J Comp Neurol 287:422–445. https://doi.org/10.1002/cne.902870403
Chau T, Ji JP, Tam C, Schwellnus H (2006) A novel instrument for quantifying grip activity during handwriting. Arch Phys Med Rehab 87:1542–1547. https://doi.org/10.1016/j.apmr.2006.08.328
Danna J, Velay JL (2015) Basic and supplementary sensory feedback in handwriting. Front Psychol 6:169. https://doi.org/10.3389/fpsyg.2015.00169
Danna J, Velay JL (2017) On the auditory-proprioception substitution hypothesis: movement sonification in two deafferented subjects learning to write new graphic patterns. Front Neurosci 11:137. https://doi.org/10.3389/fnins.2017.00137
Desmedt JE, Robertson D (1977) Differential enhancement of early and late components of the cerebral somatosensory evoked potentials during forced-paced cognitive tasks in man. J Physiol 271:761–782. https://doi.org/10.1113/jphysiol.1977.sp012025
Ebied AM, Kemp GJ, Frostick SP (2004) The role of cutaneous sensation in the motor function of the hand. J Orthop Res 22:862–866. https://doi.org/10.1016/j.orthres.2003.12.005
Fabre M, Antoine M, Germain Robitaille M, Ribot-Ciscar E, Ackerley R, Aimonetti JM, Chavet P, Blouin J, Simoneau M, Mouchnino L (2021) Large postural sways prevent foot tactile information from fading: neurophysiological evidence. Cereb Cortex Comm 2:1–10. https://doi.org/10.1093/texcom/tgaa094
Friedman DP, Murray EA, O’Neill JB, Mishkin M (1986) Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch. Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch. J Comp Neurol 252:323–347. https://doi.org/10.1002/cne.902520304
Handrigan GA, Berrigan F, Hue O, Simoneau M, Corbeil P, Tremblay A, Teasdale N (2012) The effects of muscle strength on center of pressure-based measures of postural sway in obese and heavy athletic individuals. Gait Posture 35:88–91. https://doi.org/10.1016/j.gaitpost.2011.08.012
Hepp-Reymond MC, Chakarov V, Schulte-Mönting J, Huethe F, Kristeva R (2009) Role of proprioception and vision in handwriting. Brain Res Bull 79:365–370. https://doi.org/10.1016/j.brainresbull.2009.05.013
Hermsdörfer J, Marquardt C, Schneider AS, Fürholzer W, Baur B (2011) Significance of finger forces and kinematics during handwriting in writer’s cramp. Hum Mov Sci 30:807–817. https://doi.org/10.1016/j.humov.2010.04.004
Huang Y, Parra LC, Haufe S (2016) The New York head-a precise standardized volume conductor model for EEG source localization and tES targeting. Neuroimage 140:150–162. https://doi.org/10.1016/j.neuroimage.2015.12.019
Johansson RS, Flanagan JR (2009) Coding and use of tactile signals from the fingertips in object manipulation tasks. Nat Rev Neurosci 10:345–359. https://doi.org/10.1038/nrn2621
Johansson RS, Vallbo AB (1983) Tactile sensory coding in the glabrous skin of the human hand. Trends Neurosci 6:27–32. https://doi.org/10.1016/0166-2236(83)90011-5
Johansson RS, Westling G (1984) Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects. Exp Brain Res 56:550–564. https://doi.org/10.1007/BF00237997
Kennedy PM, Inglis T (2002) Distribution and behaviour of glabrous cutaneous receptors in the human foot sole. J Physiol 538:995–1002. https://doi.org/10.1113/jphysiol.2001.013087
Knellwolf TP, Burton AR, Hammam E, Macefield VG (2018) Microneurography from the posterior tibial nerve: a novel method of recording activity from the foot in freely standing humans. J Neurophysiol 120:953–959. https://doi.org/10.1152/jn.00937
Knibestöl M (1975) Stimulus-response functions of slowly adapting mechanoreceptors in the human glabrous skin area. J Physiol (Lond) 245:63–80
Koziatek SM, Powell NJ (2003) Pencil grips, legibility, and speed of fourth-graders’ writing in cursive. Am J Occup Ther 57:284–288
Lhomond O, Teasdale N, Simoneau M, Mouchnino L (2016) Neural consequences of increasing body weight: evidence from somatosensory evoked potentials and the frequency-specificity of brain oscillations. Front Hum Neurosci 10:318. https://doi.org/10.3389/fnhum.2016.00318
Lin YC, Chao YL, Wu SK, Lin HH, Hsu CH, Hsu HM, Kuo LC (2017) Comprehension of handwriting development: pen-grip kinetics in handwriting tasks and its relation to fine motor skills among school-age children. Aust Occup Ther J 64:369–380. https://doi.org/10.1111/1440-1630.12393
Macefield VG (2005) Physiological characteristics of low-threshold mechanoreceptors in joints, muscle and skin in human subjects. Clinic Exp Pharmacol Physiol 32:135–144. https://doi.org/10.1111/j.1440-1681.2005.04143.x
Macuga KL, Frey SH (2014) Differential contributions of the superior and inferior parietal cortex to feedback versus feedforward control of tools. Neuroimage 92:36–45. https://doi.org/10.1016/j.neuroimage.2014.01.024
Mosher JC, Leahy RM, Lewis PS (1999) EEG and MEG: forward solutions for inverse methods. IEEE Trans Biomed Eng 46:245–259. https://doi.org/10.1109/10.748978
Naceri A, Gultekin YB, Moscatelli A, Ernst MO (2021) Role of tactile noise in the control of digit normal force. Front Psychol 12:612558. https://doi.org/10.3389/fpsyg.2021.612558
Northoff G, Bermpohl F (2004) Cortical midline structures and the self. Trends Cogn Sci 8:102–107. https://doi.org/10.1016/j.tics.2004.01.004
Padberg J, Cerkevich C, Engle J, Rajan AT, Recanzone G, Kaas J, Krubitzer L (2009) Thalamocortical connections of parietal somatosensory cortical fields in macaque monkeys are highly divergent and convergent. Cereb Cortex 19:2038–2064. https://doi.org/10.1093/cercor/bhn229
Parush S, Levanon-Erez N, Weintraub N (1998) Ergonomic factors influencing handwriting performance. Work 11:295–305. https://doi.org/10.3233/WOR-1998-11306
Pearson RC, Brodal P, Powell TP (1978) The projection of the thalamus upon the parietal lobe in the monkey. Brain Res 144:143–148. https://doi.org/10.1016/0006-8993(78)90440-7
Pons TP, Kaas JH (1985) Connections of area 2 of somatosensory cortex with the anterior pulvinar and subdivisions of the ventroposterior complex in macaque monkeys. J Comp Neurol 240:16–36. https://doi.org/10.1002/cne.902400103
Rosenblum S, Goldstand S, Parush S (2006) Relationships among biomechanical ergonomic factors, handwriting product quality, handwriting efficiency, and computerized handwriting process measures in children with and without handwriting difficulties. Am J Occup Ther 60:28–39. https://doi.org/10.5014/ajot.60.1.28
Ruby P, Decety J (2001) Effect of subjective perspective taking during simulation of action: a PET investigation of agency. Nat Neurosci 4:546–550. https://doi.org/10.1038/87510
Schneck CM (1991) Comparison of pencil-grip patterns in first graders with good and poor writing skills. Am J Occup Ther 45:701–706. https://doi.org/10.5014/ajot.45.8.701
Schwellnus H, Carnahan H, Kushki A, Polatajko H, Missiuna C, Chau T (2012) Effect of pencil grasp on the speed and legibility of handwriting in children. Am J Occup Ther 66:718–726
Seki K, Perlmutter SI, Fetz EE (2003) Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nat Neurosci 6:1309–1316. https://doi.org/10.1038/nn1154
Shah LJ, Gladson BL (2015) The relationship of pencil grasp on college students’ handwriting speed and legibility. J Occup Ther Sch Early Interv 8:180–191
Smits-Engelsman BCM, Wilson PH, Westenberg Y, Duysens J (2003) Fine motor deficiencies in children with developmental coordination disorder and learning disabilities: an underlying open-loop control deficit. Hum Mov Sci 22:495–513. https://doi.org/10.1016/j.humov.2003.09.006
Tadel F, Baillet S, Mosher JC, Pantazis D, Leahy RM (2011) Brainstorm: a user-friendly application for MEG/EEG analysis. Comput Intel Neurosci. https://doi.org/10.1155/2011/879716
Teasdale N, Forget R, Bard C, Paillard J, Fleury M, Lamarre Y (1993) The role of proprioceptive information for the production of isometric forces and for handwriting tasks. Acta Psychol 82:179–191. https://doi.org/10.1016/0001-6918(93)90011-F
Trulsson M (2001) Mechanoreceptive afferents in the human sural nerve. Exp Brain Res 137(1):111–116. https://doi.org/10.1007/s002210000649
Vallbo AB, Olausson H, Wessberg J, Kakuda N (1995) Receptive field characteristics of tactile units with myelinated afferents in hairy skin of human subjects. J Physiol 483:783–795. https://doi.org/10.1113/jphysiol.1995.sp020622
Van Gemmert ARA, van Galen GP (1997) Stress, neuromotor noise, and human performance: a theoretical perspective. J Exp Psychol Human 23:1299–1313. https://doi.org/10.1037/0096-1523.23.5.1299
Vedel JP, Roll JP (1982) Response to pressure and vibration of slowly adapting cutaneous mechanoreceptors in the human foot. Neurosci Lett 34:289–294. https://doi.org/10.1016/0304-3940(82)90190-2
Vela SA, Lavery LA, Armstrong DG, Anaim AA (1998) The effect of increased weight on peak pressures: implications for obesity and diabetic foot pathology. J Foot Ankle Surg 37:416–420. https://doi.org/10.1016/s1067-2516(98)80051-3
Von Holst E, Mittelstaedt H (1950) Das reafferenzprinzip. Naturwissenschaften 37:464–476. https://doi.org/10.1007/BF00622503
Voss M, Ingram JN, Haggard P, Wolpert DM (2006) Sensorimotor attenuation by central motor command signals in the absence of movement. Nat Neurosci 9:26–27. https://doi.org/10.1038/nn1592
White O, Davare M, Andres M, Olivier E (2013) The role of left supplementary motor area in grip force scaling. PLoS ONE 8(12):e83812. https://doi.org/10.1371/journal.pone.0083812
Williams SR, Chapman CE (2002) Time course and magnitude of movement-related gating of tactile detection in humans. III. Effect of motor tasks. J Neurophysiol 88:1968–1979. https://doi.org/10.1152/jn.2002.88.4.1968
Wolpert DM, Goodbody SJ, Husain M (1998) Maintaining internal representations: the role of the human superior parietal lobe. Nat Neurosci 1:529–233. https://doi.org/10.1038/2245
Wright WG, Ivanenko YP, Gurfinkel VS (2012) Foot anatomy specialization for postural sensation and control. J Neurophysiol 107:1513–1521. https://doi.org/10.1152/jn.00256.2011
Zatsiorsky VM, Li ZM, Latash ML (2000) Enslaving effects in multi-finger force production. Exp Brain Res 131:187–195. https://doi.org/10.1007/s002219900261
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The authors would like to thank David Wood (English at your Service, www.eays.eu) for revising the English of the paper.
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This work was supported by the DefiAuton CNRS project and the French National Research Agency ANR grant “COMTACT” (ANR-20-CE28-0010). This work was carried out within the Institut Convergence ILCB (ANR-16-CONV-0002).
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JD: Conceptualization, methodology, data acquisition, data analysis, writing–original draft preparation. MN: data acquisition, data analysis. DL: methodology. SM: methodology. LM: conceptualization, methodology, data acquisition, data analysis, writing–reviewing and editing.
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Danna, J., Nordlund, M., Louber, D. et al. Overpressure on fingertips prevents state estimation of the pen grip force and movement accuracy. Exp Brain Res 240, 189–198 (2022). https://doi.org/10.1007/s00221-021-06246-x
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DOI: https://doi.org/10.1007/s00221-021-06246-x