Combined action observation and imagery facilitates corticospinal excitability

David J Wright, Jacqueline Williams, Paul S Holmes, David J Wright, Jacqueline Williams, Paul S Holmes

Abstract

Observation and imagery of movement both activate similar brain regions to those involved in movement execution. As such, both are recommended as techniques for aiding the recovery of motor function following stroke. Traditionally, action observation and movement imagery (MI) have been considered as independent intervention techniques. Researchers have however begun to consider the possibility of combining the two techniques into a single intervention strategy. This study investigated the effect of combined action observation and MI on corticospinal excitability, in comparison to either observation or imagery alone. Single-pulse transcranial magnetic stimulation (TMS) was delivered to the hand representation of the left motor cortex during combined action observation and MI, passive observation (PO), or MI of right index finger abduction-adduction movements or control conditions. Motor evoked potentials (MEPs) were recorded from the first dorsal interosseous (FDI) and abductor digiti minimi (ADM) muscles of the right hand. The combined action observation and MI condition produced MEPs of larger amplitude than were obtained during PO and control conditions. This effect was only present in the FDI muscle, indicating the facilitation of corticospinal excitability during the combined condition was specific to the muscles involved in the observed/imagined task. These findings have implications for stroke rehabilitation, where combined action observation and MI interventions may prove to be more effective than observation or imagery alone.

Keywords: action observation; motor evoked potentials; movement imagery; stroke rehabilitation; transcranial magnetic stimulation.

Figures

Figure 1
Figure 1
A schematic representation of the six conditions in the experiment. All videos were 9000 ms duration and one stimulation was delivered per trial at either 3500 or 8000 ms. An auditory metronome was present during the Backward Counting (BC) and Movement Imagery (MI) conditions.
Figure 2
Figure 2
Mean MEP amplitudes, displayed asz-scores, recorded from all six conditions for (A) the right FDI muscle and (B) the right ADM muscle. Asterisks indicate significant differences between conditions.

References

    1. Aglioti S. M., Cesari P., Romani M., Urgesi C. (2008). Action anticipation and motor resonance in elite basketball players. Nat. Neurosci. 11, 1109–1116. 10.1038/nn.2182
    1. Andres M., Olivier E., Badets A. (2008). Actions, words and numbers: a contribution to semantic processing?. Curr. Dir. Psychol. Sci. 17, 313–317 10.1111/j.1467-8721.2008.00597.x
    1. Andres M., Seron X., Olivier E. (2007). Contribution of hand motor circuits to counting. J. Cogn. Neurosci. 19, 563–576. 10.1162/jocn.2007.19.4.563
    1. Berends H. I., Wolkorte R., Ijzerman M. J., van Putten M. J. A. M. (2013). Differential cortical activation during observation and observation-and-imagination. Exp. Brain Res. 229, 337–345. 10.1007/s00221-013-3571-8
    1. Borroni P., Montagna M., Cerri G., Baldissera F. (2005). Cyclic time course of motor excitability modulation during the observation of a cyclic hand movement. Brain Res. 1065, 115–124. 10.1016/j.brainres.2005.10.034
    1. Brasil-Neto J. P., Cohen L. G., Panizza M., Nilsson J., Roth B. J., Hallett M. (1992). Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse and stimulus intensity. J. Clin. Neurophysiol. 9, 132–136. 10.1097/00004691-199201000-00014
    1. Buccino G., Vogt S., Ritzl A., Fink G. R., Zilles K., Freund H. J., et al. . (2004). Neural circuits underlying imitation learning of hand actions: an event-related fMRI study. Neuron 42, 323–334. 10.1016/S0896-6273(04)00181-3
    1. Clark S., Tremblay F., Ste-Marie D. (2004). Differential modulation of corticospinal excitability during observation, mental imagery and imitation of hand actions. Neuropsychologia 42, 105–112. 10.1016/s0028-3932(03)00144-1
    1. Declaration of Helsinki . (2013). World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 310, 2191–2194. 10.1001/jama.2013.281053
    1. de Vries S., Mulder T. (2007). Motor imagery and stroke rehabilitation: a critical discussion. J. Rehabil. Med. 39, 5–13. 10.2340/16501977-0020
    1. Eaves D. L., Haythornthwaite L., Vogt S. (2014). Motor imagery during action observation modulates automatic imitation effects in rhythmical actions. Front. Hum. Neurosci. 8:28. 10.3389/fnhum.2014.00028
    1. Ertelt D., Small S., Solodkin A., Dettmers C., McNamara A., Binkofski F., et al. . (2007). Action observation has a positive impact on rehabilitation of motor deficits after stroke. Neuroimage 36, T164–T173. 10.1016/j.neuroimage.2007.03.043
    1. Facchini S., Muellbacher W., Battaglia F., Boroojerdi B., Hallett M. (2002). Focal enhancement of motor cortex excitability during motor imagery: a transcranial magnetic stimulation study. Acta Neurol. Scand. 105, 146–151. 10.1034/j.1600-0404.2002.1o004.x
    1. Fadiga L., Buccino G., Craighero L., Fogassi L., Gallese V., Pavesi G. (1999). Corticospinal excitability is specifically modulated by motor imagery: a magnetic stimulation study. Neuropsychologia 37, 147–158. 10.1016/S0028-3932(98)00089-X
    1. Fadiga L., Craighero L., Olivier E. (2005). Human motor cortex excitability during the perception of others’ action. Curr. Opin. Neurobiol. 15, 213–218. 10.1016/j.conb.2005.03.013
    1. Fadiga L., Fogassi L., Pavesi G., Rizzolatti G. (1995). Motor facilitation during action observation: a magnetic stimulation study. J. Neurophysiol. 73, 2608–2611.
    1. Filimon F., Nelson J. D., Hagler D. J., Sereno M. I. (2007). Human cortical representations for reaching: mirror neurons for execution, observation and imagery. Neuroimage 37, 1315–1328. 10.1016/j.neuroimage.2007.06.008
    1. Frey S. H., Gerry V. E. (2006). Modulation neural activity during observational learning of actions and their sequential orders. J. Neurosci. 26, 13194–13201. 10.1523/JNEUROSCI.3914-06.2006
    1. Grahn J. A., Brett M. (2007). Rhythm and beat perception in the motor areas of the brain. J. Cogn. Neurosci. 19, 893–906. 10.1162/jocn.2007.19.5.893
    1. Grèzes J., Costes N., Decety J. (1999). The effects of learning and intention on the neural network involved in the perception of meaningless actions. Brain 122, 1875–1887. 10.1093/brain/122.10.1875
    1. Grèzes J., Decety J. (2001). Functional anatomy of execution, mental simulation, observation and verb generation of actions: a meta-analysis. Hum. Brain Mapp. 12, 1–19. 10.1002/1097-0193(200101)12:1<01::AID-HBM10>;2-V
    1. Hashimoto R., Rothwell J. C. (1999). Dynamic changes in corticospinal excitability during motor imagery. Exp. Brain Res. 125, 75–81. 10.1007/s002210050660
    1. Holmes P., Calmels C. (2008). A neuroscientific review of imagery and observation use in sport. J. Mot. Behav. 40, 433–445. 10.3200/JMBR.40.5.433-445
    1. Holmes P., Ewan L. (2007). The use of structured observation as a stroke rehabilitation aid: an opinion from neuroscience. Brit. J. Occupat. Ther. 70, 454–456.
    1. Kasai T., Kawai S., Kawanishi M., Yahagi S. (1997). Evidence for facilitation of motor evoked potentials (MEPs) induced by motor imagery. Brain Res. 744, 147–150. 10.1016/S0006-8993(96)01101-8
    1. Keel J. C., Smith M. J., Wassermann E. M. (2001). A safety screening questionnaire for transcranial magnetic stimulation. Clin. Neurophysiol. 112:720. 10.1016/S1388-2457(00)00518-6
    1. Léonard G., Tremblay F. (2007). Corticomotor facilitation associated with observation, imagery and imitation of hand actions: a comparative study in young and old adults. Exp. Brain Res. 177, 167–175. 10.1007/s00221-006-0657-6
    1. Loporto M., Holmes P. S., Wright D. J., McAllister C. J. (2013). Reflecting on mirror mechanisms: motor resonance effects during action observation only present with low-intensity transcranial magnetic stimulation. PLoS One 8:e64911. 10.1371/journal.pone.0064911
    1. Loporto M., McAllister C. J., Edwards M. G., Wright D. J., Holmes P. S. (2012). Prior action execution has no effect on corticospinal facilitation during action observation. Behav. Brain Res. 231, 124–129. 10.1016/j.bbr.2012.03.009
    1. Loporto M., McAllister C., Williams J., Hardwick R., Holmes P. (2011). Investigating central mechanisms underlying the effects of action observation and imagery through transcranial magnetic stimuluation. J. Motor. Behav. 43, 361–373. 10.1080/00222895.2011.604655
    1. Macuga K. L., Frey S. H. (2012). Neural representations involved in observed, imagined and imitated actions are dissociable and hierarchically organized. Neuroimage 59, 2798–2807. 10.1016/j.neuroimage.2011.09.083
    1. Mulder T. (2007). Motor imagery and action observation: cognitive tools for rehabilitation. J. Neural Transm. 114, 1265–1278. 10.1007/s00702-007-0763-z
    1. Munzert J., Zentgraf K., Stark R., Vaitl D. (2008). Neural activation in cognitive motor processes: comparing motor imagery and observation of gymnastic movements. Exp. Brain Res. 188, 437–444. 10.1007/s00221-008-1376-y
    1. Naish K. R., Houston-Price C., Bremner A. J., Holmes N. P. (2014). Effects of action observation on corticospinal excitability: muscle specificity, direction and timing of the mirror response. Neuropsychologia [Epub ahead of print]. 64, 331–348. 10.1016/j.neuropsychologia.2014.09.034
    1. Nedelko V., Hassa T., Hamzei F., Schoenfeld M. A., Dettmers C. (2012). Action imagery combined with action observation activates more corticomotor regions than action observation alone. J. Neurol. Phys. Ther. 36, 182–188. 10.1097/NPT.0b013e318272cad1
    1. Ohno K., Higashi T., Sugawara K., Ogahara K., Funase K., Kasai T. (2011). Excitability changes in the human primary motor cortex during observation with motor imagery of chopstick use. J. Physical Ther. Sci. 23, 703–706 10.1589/jpts.23.703
    1. Oldfield R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113. 10.1016/0028-3932(71)90067-4
    1. Patuzzo S., Fiaschi A., Manganotti P. (2003). Modulation of motor cortex excitability in the left hemisphere during action observation: a single- and paired-pulse transcranial magnetic stimulation study of self- and non-self-action observation. Neuropsychologia 41, 1272–1278. 10.1016/S0028-3932(02)00293-2
    1. Petersen N. T., Pyndt H. S., Nielsen J. B. (2003). Investigating human motor control by transcranial magnetic stimulation. Exp. Brain Res. 152, 1–16. 10.1007/s00221-003-1537-y
    1. Rizzolatti G. (2005). The mirron neuron system and its function in humans. Anat. Embryol. (Berl) 210, 419–421. 10.1007/s00429-005-0039-z
    1. Rizzolatti G., Craighero L. (2004). The mirror-neuron system. Annu. Rev. Neurosci. 27, 169–192. 10.1146/annurev.neuro.27.070203.144230
    1. Roberts R., Callow N., Hardy L., Markland D., Bringer J. (2008). Movement imagery ability: development and assessment of a revised version of the vividness of movement imagery questionnaire. J. Sport Exerc. Psychol. 30, 200–221.
    1. Roosink M., Zijdewind I. (2010). Corticospinal excitability during observation and imagery of simple and complex hand tasks: implications for motor rehabilitation. Behav. Brain Res. 213, 35–41. 10.1016/j.bbr.2010.04.027
    1. Rossini P. M., Barker A. T., Berardelli A., Caramia M. D., Caruso G., Cracco R. Q., et al. . (1994). Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr. Clin. Neurophysiol. 91, 79–92. 10.1016/0013-4694(94)90029-9
    1. Rossini P. M., Rossi S., Pasqualetti P., Tecchio F. (1999). Corticospinal excitability modulation to hand muscles during movement imagery. Cereb. Cortex 9, 161–167. 10.1093/cercor/9.2.161
    1. Rothwell J. C. (1997). Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J. Neurosci. Methods 74, 113–122. 10.1016/S0165-0270(97)02242-5
    1. Sakamoto M., Muraoka T., Mizuguchi N., Kanosue K. (2009). Combining observation and imagery of an action enhances human corticospinal excitability. Neurosci. Res. 65, 23–27. 10.1016/j.neures.2009.05.003
    1. Sharma N., Pomeroy V. M., Baron J. C. (2006). Motor imagery: a backdoor to the motor after stroke? Stroke 37, 1941–1952. 10.1161/01.STR.0000226902.43357.fc
    1. Stinear C. M., Byblow W. D., Steyvers M., Levin O., Swinnen S. P. (2006). Kinesthetic, but not visual, motor imagery modulates corticomotor excitability. Exp. Brain Res. 168, 157–164. 10.1007/s00221-005-0078-y
    1. Strafella A. P., Paus T. (2000). Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. Neuroreport 11, 2289–2292. 10.1097/00001756-200007140-00044
    1. Tsukazaki I., Uehara K., Morishita T., Ninomiya M., Funase K. (2012). Effect of observation combined with motor imagery of a skilled hand-motor task on motor cortical excitability: difference between novice and expert. Neurosci. Lett. 518, 96–100. 10.1016/j.neulet.2012.04.061
    1. Villiger M., Estévez N., Hepp-Raymond M. C., Kiper D., Kollias S. S., Eng K., et al. . (2013). Enhanced activation of motor execution networks using action observation combined with imagination of lower limb movements. PLoS One 8:e72403. 10.1371/journal.pone.0072403
    1. Vogt S., Di Rienzo F., Collet C., Collins A., Guillot A. (2013). Multiple roles of motor imagery during action observation. Front. Hum. Neurosci. 7:807. 10.3389/fnhum.2013.00807
    1. Williams J., Pearce A. J., Loporto M., Morris T., Holmes P. S. (2012). The relationship between corticospinal excitability during motor imagery and motor imagery ability. Behav. Brain Res. 226, 369–375. 10.1016/j.bbr.2011.09.014

Source: PubMed

赞助者和合作者

医疗条件

药物干预

3
订阅