Induction of Long-term Depression-like Plasticity by Pairings of Motor Imagination and Peripheral Electrical Stimulation

Mads Jochumsen, Nada Signal, Rasmus W Nedergaard, Denise Taylor, Heidi Haavik, Imran K Niazi, Mads Jochumsen, Nada Signal, Rasmus W Nedergaard, Denise Taylor, Heidi Haavik, Imran K Niazi

Abstract

Long-term depression (LTD) and long-term potentiation (LTP)-like plasticity are models of synaptic plasticity which have been associated with memory and learning. The induction of LTD and LTP-like plasticity, using different stimulation protocols, has been proposed as a means of addressing abnormalities in cortical excitability associated with conditions such as focal hand dystonia and stroke. The aim of this study was to investigate whether the excitability of the cortical projections to the tibialis anterior (TA) muscle could be decreased when dorsiflexion of the ankle joint was imagined and paired with peripheral electrical stimulation (ES) of the nerve supplying the antagonist soleus muscle. The effect of stimulus timing was evaluated by comparing paired stimulation timed to reach the cortex before, at and after the onset of imagined movement. Fourteen healthy subjects participated in six experimental sessions held on non-consecutive days. The timing of stimulation delivery was determined offline based on the contingent negative variation (CNV) of electroencephalography brain data obtained during imagined dorsiflexion. Afferent stimulation was provided via a single pulse ES to the peripheral nerve paired, based on the CNV, with motor imagination of ankle dorsiflexion. A significant decrease (P = 0.001) in the excitability of the cortical projection of TA was observed when the afferent volley from the ES of the tibial nerve (TN) reached the cortex at the onset of motor imagination based on the CNV. When TN stimulation was delivered before (P = 0.62), or after (P = 0.23) imagined movement onset there was no significant effect. Nor was a significant effect found when ES of the TN was applied independent of imagined movement (P = 0.45). Therefore, the excitability of the cortical projection to a muscle can be inhibited when ES of the nerve supplying the antagonist muscle is precisely paired with the onset of imagined movement.

Keywords: associative stimulation; brain plasticity; contingent negative variation; cortical excitability; long-term depression; long-term potentiation; motor imagination.

Figures

FIGURE 1
FIGURE 1
The visual cue is presented in the top graph. It was used in Sessions 1–5. An example of the contingent negative variation (CNV) is shown in the bottom graph.
FIGURE 2
FIGURE 2
The raw averaged motor evoked potential (MEPs) for the transcranial magnetic stimulation (TMS) intensities are shown for the three main interventions on the left side of the figure (averaged across all subjects). On the right site of the figure, the timing of the ES according to the three phases of the CNV (average across all subjects) is shown.
FIGURE 3
FIGURE 3
The averaged (across subjects) MEPmax is shown for each of the main interventions (Before, At and and After the onset of motor imagination) and control experiments (CPN stimulation at the onset of motor imagination and TN alone). 0% change with respect to the baseline means no change from the pre- to post-intervention measurements. ‘∗’ indicates a significant difference in the MEPmax from the pre- to post-intervention measurements.

References

    1. Abbruzzese G., Assini A., Buccolieri A., Marchese R., Trompetto C. (1999). Changes of intracortical inhibition during motor imagery in human subjects. Neurosci. Lett. 263 113–116. 10.1016/S0304-3940(99)00120-2
    1. Byl N. N. (2007). Learning-based animal models: task-specific focal hand dystonia. ILAR J. 48 411–431. 10.1093/ilar.48.4.411
    1. Castel-Lacanal E., Marque P., Tardy J., De Boissezon X., Guiraud V., Chollet F., et al. (2009). Induction of cortical plastic changes in wrist muscles by paired associative stimulation in the recovery phase of stroke patients. Neurorehabil. Neural Repair 23 366–372. 10.1177/1545968308322841
    1. Chen R., Classen J., Gerloff C., Celnik P., Wassermann E. M., Hallett M., et al. (1997). Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48 1398–1403. 10.1212/WNL.48.5.1398
    1. Chipchase L., Schaburn S., Hodges P. (2011). Peripheral electrical stimulation to induce cortical plasticity: a systematic review of stimulus parameters. Clin. Neurophysiol. 122 456–463. 10.1016/j.clinph.2010.07.025
    1. Chisari C., Fanciullacci C., Lamola G., Rossi B., Cohen L. G. (2014). Nibs-driven brain plasticity. Arch. Ital. Biol. 152 247–258. 10.12871/00039829201445
    1. Collingridge G. L., Peineau S., Howland J. G., Wang Y. T. (2010). Long-term depression in the Cns. Nat. Rev. Neurosci. 11 459–473. 10.1038/nrn2867
    1. de Vries S., Mulder T. (2007). Motor imagery and stroke rehabilitation: a critical discussion. Acta Derm. Venereol. 39 5–13. 10.2340/16501977-0020
    1. Devanne H., Lavoie B. A., Capaday C. (1997). Input-output properties and gain changes in the human corticospinal pathway. Exp. Brain Res. 114 329–338. 10.1007/PL00005641
    1. Dietz V., Sinkjaer T. (2007). Spastic movement disorder: impaired reflex function and altered muscle mechanics. Lancet Neurol. 6 725–733. 10.1016/S1474-4422(07)70193-X
    1. Hebb D. O. (1949). The Organization of Behavior: A Neuropsychological Theory, New Edn. New York, NY: Wiley.
    1. Kang J. S., Terranova C., Hilker R., Quartarone A., Ziemann U. (2011). Deficient homeostatic regulation of practice-dependent plasticity in writer’s cramp. Cereb. Cortex 21 1203–1212. 10.1093/cercor/bhq204
    1. Khaslavskaia S., Ladouceur M., Sinkjaer T. (2002). Increase in tibialis anterior motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve. Exp. Brain Res. 145 309–315. 10.1007/s00221-002-1094-9
    1. Khaslavskaia S., Sinkjaer T. (2005). Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive. Exp. Brain Res. 162 497–502. 10.1007/s00221-004-2153-1
    1. Kumpulainen S., Mrachacz-Kersting N., Peltonen J., Voigt M., Avela J. (2012). The optimal interstimulus interval and repeatability of paired associative stimulation when the soleus muscle is targeted. Exp. Brain Res. 221 241–249. 10.1007/s00221-012-3165-x
    1. Lu M., Arai N., Tsai C., Ziemann U. (2011). Movement related cortical potentials of cued versus self-initiated movements: double dissociated modulation by dorsal premotor cortex versus supplementary motor area rtms. Hum. Brain Mapp. 33 824–839.
    1. Malenka R. C., Bear M. F. (2004). Ltp and Ltd: an embarrassment of riches. Neuron 44 5–21. 10.1016/j.neuron.2004.09.012
    1. Mrachacz-Kersting N., Fong M., Murphy B. A., Sinkjær T. (2007). Changes in excitability of the cortical projections to the human tibialis anterior after paired associative stimulation. J. Neurophysiol. 97 1951–1958. 10.1152/jn.01176.2006
    1. Mrachacz-Kersting N., Kristensen S. R., Niazi I. K., Farina D. (2012). Precise temporal association between cortical potentials evoked by motor imagination and afference induces cortical plasticity. J. Physiol. 590 1669–1682. 10.1113/jphysiol.2011.222851
    1. Niazi I. K., Kersting N. M., Jiang N., Dremstrup K., Farina D. (2012). Peripheral electrical stimulation triggered by self-paced detection of motor intention enhances motor evoked potentials. IEEE Trans. Neural Syst. Rehabil. Eng. 20 595–604. 10.1109/TNSRE.2012.2194309
    1. Nitsche M. A., Paulus W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. 527(Pt 3) 633–639. 10.1111/j.1469-7793.2000.t01-1-00633.x
    1. Pascual Leone A., Amedi A., Fregni F., Merabet L. B. (2005). The plastic human brain cortex. Annu. Rev. Neurosci. 28 377–401. 10.1146/annurev.neuro.27.070203.144216
    1. Pascual-Leone A., Dang N., Cohen L. G., Brasil-Neto J. P., Cammarota A., Hallett M. (1995). Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J. Neurophysiol. 74 1037–1045.
    1. Pascual-Leone A., Valls-Sole J., Wassermann E. M., Hallett M. (1994). Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117(Pt 4) 847–858. 10.1093/brain/117.4.847
    1. Pavlides C., Miyashita E., Asanuma H. (1993). Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. J. Neurophysiol. 70 733–741.
    1. Quartarone A., Rizzo V., Bagnato S., Morgante F., Sant’angelo A., Romano M., et al. (2005). Homeostatic-like plasticity of the primary motor hand area is impaired in focal hand dystonia. Brain 128(Pt 8) 1943–1950. 10.1093/brain/awh527
    1. Rossi S., Hallett M., Rossini P. M., Pascual-Leone A. (2009). Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol. 120 2008–2039. 10.1016/j.clinph.2009.08.016
    1. Schabrun S. M., Ridding M. C., Galea M. P., Hodges P. W., Chipchase L. S. (2012). Primary sensory and motor cortex excitability are co-modulated in response to peripheral electrical nerve stimulation. PLoS ONE 7:51298 10.1371/journal.pone.0051298
    1. Shibasaki H., Hallett M. (2006). What is the Bereitschaftspotential? Clin. Neurophysiol. 117 2341–2356. 10.1016/j.clinph.2006.04.025
    1. Sjostrom P. J., Rancz E. A., Roth A., Hausser M. (2008). Dendritic excitability and synaptic plasticity. Physiol. Rev. 88 769–840. 10.1152/physrev.00016.2007
    1. Stefan K., Gentner R., Zeller D., Dang S., Classen J. (2008). Theta-burst stimulation: remote physiological and local behavioral after-effects. Neuroimage 40 265–274. 10.1016/j.neuroimage.2007.11.037
    1. Stefan K., Kunesch E., Cohen L. G., Benecke R., Classen J. (2000). Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123 572–584. 10.1093/brain/123.3.572
    1. Stent G. S. (1973). A physiological mechanism for Hebb’s postulate of learning. Proc. Natl. Acad. Sci. U.S.A. 70 997–1001. 10.1073/pnas.70.4.997
    1. Walter W. G., Cooper R., Aldridge V. J., Mccallum W. C., Winter A. L. (1964). Contingent negative variation: an electric sign of sensorimotor association and expectancy in the human brain. Nature (Lond.) 203 380–384. 10.1038/203380a0
    1. Weise D., Schramm A., Stefan K., Wolters A., Reiners K., Naumann M., et al. (2006). The two sides of associative plasticity in writer’s cramp. Brain 129(Pt 10) 2709–2721. 10.1093/brain/awl221
    1. Wolters A., Sandbrink F., Schlottmann A., Kunesch E., Stefan K., Cohen L. G., et al. (2003). A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J. Neurophysiol. 89 2339–2345. 10.1152/jn.00900.2002
    1. Ziemann U., Ilic T. V., Pauli C., Meintzschel F., Ruge D. (2004). Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J. Neurosci. 24 1666–1672. 10.1523/JNEUROSCI.5016-03.2004

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