Abstract
The purpose of this study was to investigate the role of cutaneous feedback in the agonist–antagonist co-activation mechanism during maximum voluntary force (MVF) production by the fingers. Seventeen healthy male subjects (age: 23.8 ± 1.0 years) were asked to press with maximal effort at their fingertips. Finger forces at the fingertips and muscle activities of the flexor digitorum superficialis (FDS, agonist) and extensor digitorum communis (EDC, antagonist) were recorded using force sensors and electromyography, respectively. There were two experimental conditions: with and without administration of a ring block to the fingers (i.e., anesthesia and normal conditions, or AC and NC, respectively). The ring block was used to deprive cutaneous feedback. Consistent with previous studies, finger MVF decreased significantly in AC compared with NC. Moreover, the force production of non-task fingers significantly increased in AC. Muscle activity of the EDC was significantly lower in AC than in NC; no significant changes in the FDS muscle were observed. The findings of this study show that cutaneous feedback not only increases MVF and force accuracy, but facilitates agonist–antagonist co-activation by increasing antagonist muscle activation. The results of this study imply that cutaneous feedback is linked to both primary and adjacent motor neurons.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Acsády L, Görcs TJ, Freund TF (1996) Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience 73:317–334
Augurelle AS, Smith AM, Lejeune T, Thonnard JL (2003) Importance of cutaneous feedback in maintaining a secure grip during manipulation of hand-held objects. J Neurophysiol 89:665–671
Beck S, Hallett M (2011) Surround inhibition in the motor system. Exp Brain Res 210:165–172
Brasilneto JP, Vallssole J, Pascualleone A, Cammarota A, Amassian VE, Cracco R, Maccabee P, Cracco J, Hallett M, Cohen LG (1993) Rapid modulation of human cortical motor outputs following ischemic nerve block. Brain 116:511–525
Canedo A (1997) Primary motor cortex influences on the descending and ascending systems. Prog Neurobiol 51:287–335
Capaday C, Devanne H, Bertrand L, Lavoie BA (1998) Intracortical connections between motor cortical zones controlling antagonistic muscles in the cat: a combined anatomical and physiological study. Exp Brain Res 120:223–232
Collins DF, Knight B, Prochazka A (1999) Contact-evoked changes in EMG activity during human grasp. J Neurophysiol 81:2215–2225
Danion F, Li S, Zatsiorsky VM, Latash ML (2002) Relations between surface EMG of extrinsic flexors and individual finger forces support the notion of muscle compartments. Eur J Appl Physiol 88:185–188
Danion F, Latash ML, Li S (2003) Finger interactions studied with transcranial magnetic stimulation during multi-finger force production tasks. Clin Neurophysiol 114:1445–1455
DiDomenico A, Nussbaum MA (2008) Estimation of forces exerted by the fingers using standardised surface electromyography from the forearm. Ergonomics 51:858–871
Duque J, Vandermeeren Y, Lejeune TM, Thonnard JL, Smith AM, Olivier E (2005) Paradoxical effect of digital anaesthesia on force and corticospinal excitability. NeuroReport 16:259–262
Ernberg M, Serra E, Baad-Hansen L, Svensson P (2009) Influence of topical anaesthesia on the corticomotor response to tongue training. Arch Oral Biol 54:696–704
Ethier C, Brizzi L, Giguere D, Capaday C (2007) Corticospinal control of antagonistic muscles in the cat. Eur J Neurosci 26:1632–1641
Evrard HC, Craig AD (2008) Retrograde analysis of the cerebellar projections to the posteroventral part of the ventral lateral thalamic nucleus in the macaque monkey. J Comp Neurol 508:286–314
Gallistel CR (1981) Precis of Gallistel the organization of action. Behav Brain Sci 4:609–619
Gandevia SC, Macefield VG, Biglandritchie B, Gorman RB, Burke D (1993) Motoneuronal output and gradation of effort in attempts to contract acutely paralyzed leg muscles in man. J Physiol-Lond 471:411–427
Huijing PA, Baan GC (2003) Myofascial force transmission: muscle relative position and length determine agonist and synergist muscle force. J Appl Physiol 94:1092–1107
Jones LA, Piateski E (2006) Contribution of tactile feedback from the hand to the perception of force. Exp Brain Res 168:298–302
Kilbreath SL, Refshauge K, Gandevia SC (1997) Differential control of the digits of the human hand: evidence from digital anaesthesia and weight matching. Exp Brain Res 117:507–511
Koerber HR, Brown PB (1995) Quantitative-analysis of dorsal horn cell receptive-fields following limited deafferentation. J Neurophysiol 74:2065–2076
Nicolelis MAL, Lin RCS, Woodward DJ, Chapin JK (1993) Induction of immediate spatiotemporal changes in thalamic networks by peripheral block of ascending cutaneous information. Nature 361:533–536
Otis TS, Mody I (1992) Modulation of decay kinetics and frequency of Gaba-a receptor-mediated spontaneous inhibitory postsynaptic currents in hippocampal-neurons. Neuroscience 49:13–32
Rasmusson DD (1996) Changes in the response properties of neurons in the ventroposterior lateral thalamic nucleus of the raccoon after peripheral deafferentation. J Neurophysiol 75:2441–2450
Rossi S, Pasqualetti P, Tecchio F, Sabato N, Rossini PM (1998) Modulation of corticospinal output to human hand muscles following deprivation of sensory feedback. Neuroimage 8:163–175
Rossini PM, Rossi S, Tecchio F, Pasqualetti P, Finazzi-Agrò A, Sabato A (1996) Focal brain stimulation in healthy humans: motor maps changes following partial hand sensory deprivation. Neuroscience Lett 214:191–195
Schneider C, Devanne H, Lavoie BA, Capaday C (2002) Neural mechanisms involved in the functional linking of motor cortical points. Exp Brain Res 146:86–94
Shim JK, Olafsdottir H, Zatsiorsky VM, Latash ML (2005) The emergence and disappearance of multi-digit synergies during force-production tasks. Exp Brain Res 164:260–270
Shim JK, Karol S, Kim YS, Seo NJ, Kim YH, Kim Y, Yoon BC (2012) Tactile feedback plays a critical role in maximum finger force production. J Biomech 45:415–420
Shinoura N, Suzuki Y, Yamada R, Kodama T, Takahashi M, Yagi K (2005) Fibers connecting the primary motor and sensory areas play a role in grasp stability of the hand. Neuroimage 25:936–941
Stinear CM, Byblow WD (2003) Role of intracortical inhibition in selective hand muscle activation. J Neurophysiol 89:2014–2020
Takei T, Seki K (2010) Spinal interneurons facilitate coactivation of hand muscles during a precision grip task in monkeys. J Neurosci 30:17041–17050
Tamas G, Somogyi P, Buhl EH (1998) Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat. J Neurosci 18:4255–4270
Thomson C, Lalonde D (2006) Randomized double-blind comparison of duration of anesthesia among three commonly used agents in digital nerve block. Plast Reconstr Surg 118:429–432
Wall JT, Kaas JH, Sur M (1986) Functional reorganization in somatosensory cortical areas 3b and 1 of adult monkeys after median nerve repair: possible relationships to sensory recovery in humans. J Neurosci 6:218–233
Acknowledgments
The authors wish to thank Hyo Young Pyeon, PT, MHSc for his advice and help during the experiments. This study was supported by a Korea University grant.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kim, Y., Shim, J.K., Hong, YK. et al. Cutaneous sensory feedback plays a critical role in agonist–antagonist co-activation. Exp Brain Res 229, 149–156 (2013). https://doi.org/10.1007/s00221-013-3601-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-013-3601-6