Abstract
Dual-tasking is intrinsic to many daily activities, including walking and driving. However, the activity of the primary motor cortex (M1) in response to dual-tasks (DT) is still not well characterised. A recent meta-analysis (Corp in Neurosci Biobehav Rev 43:74–87, 2014) demonstrated a reduction in M1 inhibition during dual-tasking, yet responses were not consistent between studies. It was suggested that DT difficulty might account for some of this between-study variability. The aim of this study was to investigate whether corticospinal excitability and M1 inhibition differed between an easier and more difficult dual-task. Transcranial magnetic stimulation (TMS) was applied to participants’ abductor pollicis brevis muscle representation during a concurrent pincer grip task and stationary bike-riding. The margin of error in which to maintain pincer grip force was reduced to increase task difficulty. Compared to ST conditions, significantly increased M1 inhibition was demonstrated for the easier, but not more difficult, DT. However, there was no significant difference in M1 inhibition between easy and difficult DTs. The difference in difficulty between the two tasks may not have been wide enough to result in significant differences in M1 inhibition. Increased M1 inhibition for the easy DT condition was in opposition to the reduction in M1 inhibition found in our meta-analysis (Corp in Neurosci Biobehav Rev 43:74–87, 2014). We propose that this may be partially explained by differences in the timing of the TMS pulse between DT studies.
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Abbruzzese G, Assini A, Buccolieri A, Schieppati M, Trompetto C (1999) Comparison of intracortical inhibition and facilitation in distal and proximal arm muscles in humans. J Physiol 514:895–903
Al-Yahya E, Dawes H, Smith L, Dennis A, Howells K, Cockburn J (2011) Cognitive motor interference while walking: a systematic review and meta-analysis. Neurosci Biobehav Rev 35:715–728
Ball K, Owsley C (1991) Identifying correlates of accident involvement for the older driver. Human Factors: J Human Factors Ergon Soc 33:583–595
Beauchet O, Dubost V, Allali G, Gonthier R, Hermann FR, Kressig RW (2007) ‘Faster counting while walking’ as a predictor of falls in older adults. Age Ageing 36:418
Bherer L, Kramer A, Peterson M, Colcombe S, Erickson K, Becic E (2008) Transfer effects in task-set cost and dual-task cost after dual-task training in older and younger adults: further evidence for cognitive plasticity in attentional control in late adulthood. Exp Aging Res 34:188–219
Byblow WD, Coxon JP, Stinear CM, Fleming MK, Williams G, Müller JFM et al (2007) Functional connectivity between secondary and primary motor areas underlying hand–foot coordination. J Neurophysiol 98:414–422
Chipchase L, Schabrun S, Cohen L, Hodges P, Ridding M, Rothwell JC et al (2012) A checklist for assessing the methodological quality of studies using transcranial magnetic stimulation to study the motor system: an international consensus study. Clin Neurophysiol 123:1698–1704
Classen J, Schnitzler A, Binkofski F, Werhahn KJ, Kim Y-S, Kessler KR et al (1997) The motor syndrome associated with exaggerated inhibition within the primary motor cortex of patients with hemiparetic stroke. Brain 120:605–619
Cohen J (1977) Statistical power analysis for the behavioral sciences. Academic press, Cambridge
Corp DT, Lum JAG, Tooley GA, Pearce AJ (2014) Corticospinal activity during dual tasking: a systematic review and meta-analysis of TMS literature from 1995-2013. Neurosci Biobehav Rev 43:74–87
Dux PE, Tombu MN, Harrison S, Rogers BP, Tong F, Marois R (2009) Training improves multitasking performance by increasing the speed of information processing in human prefrontal cortex. Neuron 63:127–138
Erickson KI, Colcombe SJ, Wadhwa R, Bherer L, Peterson MS, Scalf PE et al (2005) Neural correlates of dual-task performance after minimizing task-preparation. NeuroImage 28:967–979
Field A (2009) Discovering statistics using SPSS. Sage publications, Thousand Oaks
Fuhr P, Agostino R, Hallett M (1991) Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol Evoked Potentials Sect 81:257–262
Fujiyama H, Garry M, Levin O, Swinnen SP, Summers JJ (2009) Age-related differences in inhibitory processes during interlimb coordination. Brain Res 1262:38–47
Fujiyama H, Hinder MR, Schmidt MW, Garry MI, Summers JJ (2012) Age-related differences in corticospinal excitability and inhibition during coordination of upper and lower limbs. Neurobiol Agin, 33:1484.e1481–1484.e1414
Hess C, Mills K, Murray N (1986) Magnetic stimulation of the human brain: facilitation of motor responses by voluntary contraction of ipsilateral and contralateral muscles with additional observations on an amputee. Neurosci Lett 71:235–240
Holste KG, Yasen AL, Hill M, Christie A (in press) Motor cortex inhibition is increased during a secondary cognitive task. Motor control. doi:10.1123/mc.2014-0047
Inghilleri M, Berardelli A, Cruccu G, Manfredi M (1993) Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol 466:521–534
Johansen-Berg H, Matthews P (2002) Attention to movement modulates activity in sensori-motor areas, including primary motor cortex. Exp Brain Res 142:13–24
Kahneman D (1973) Attention and effort. Prentice-Hall, New Jersey
Kidgell DJ, Pearce AJ (2010) Corticospinal properties following short-term strength training of an intrinsic hand muscle. Hum Mov Sci 29:631–641
Kujirai T, Caramia M, Rothwell JC, Day B, Thompson P, Ferbert A et al (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501–519
Li KZH, Roudaia E, Lussier M, Bherer L, Leroux A, McKinley P (2010) Benefits of cognitive dual-task training on balance performance in healthy older adults. J Gerontol Ser A Biol Sci Med Sci 65:1344
Master S, Tremblay F (2009) Task-specific increase in corticomotor excitability during tactile discrimination. Exp Brain Res 194:163–172
McIntyre-Robinson AJ, Byblow WD (2013) A neurophysiological basis for the coordination between hand and foot movement. J Neurophysiol 110:1039–1046
Owsley C, Ball K, Sloane ME, Roenker DL, Bruni JR (1991) Visual/cognitive correlates of vehicle accidents in older drivers. Psychol Aging 6:403
Pearce AJ, Thickbroom GW, Byrnes ML, Mastaglia FL (2000) Functional reorganisation of the corticomotor projection to the hand in skilled racquet players. Exp Brain Res 130:238–243
Pellecchia GL (2005) Dual-task training reduces impact of cognitive task on postural sway. J Mot Behav 37:239–246
Poston B, Kukke SN, Paine RW, Francis S, Hallett M (2012) Cortical silent period duration and its implications for surround inhibition of a hand muscle. Eur J Neurosci 36:2964–2971
Ridding M, Sheean G, Rothwell J, Inzelberg R, Kujirai T (1995) Changes in the balance between motor cortical excitation and inhibition in focal, task specific dystonia. J Neurol Neurosurg Psychiatry 59:493–498
Sherwood DE, Schmidt RA (1980) The relationship between force and force variability in minimal and near-maximal static and dynamic contractions. J Mot Behav 12:75–89
Slobounov S, Johnston J, Chiang H, Ray W (2002) Movement-related EEG potentials are force or end-effector dependent: evidence from a multi-finger experiment. Clin Neurophysiol 113:1125–1135
Slobounov S, Hallett M, Newell KM (2004) Perceived effort in force production as reflected in motor-related cortical potentials. Clin Neurophysiol 115:2391–2402
Sohn YH, Kang SY, Hallett M (2005) Corticospinal disinhibition during dual action. Exp Brain Res 162:95–99
Sugawara K, Furubayashi T, Takahashi M, Ni Z, Ugawa Y, Kasai T (2005) Remote effects of voluntary teeth clenching on excitability changes of the human hand motor area. Neurosci Lett 377:25–30
Tazoe T, Endoh T, Nakajima T, Sakamoto M, Komiyama T (2007a) Disinhibition of upper limb motor area by voluntary contraction of the lower limb muscle. Exp Brain Res 177:419–430
Tazoe T, Sakamoto M, Nakajima T, Endoh T, Komiyama T (2007b) Effects of remote muscle contraction on transcranial magnetic stimulation-induced motor evoked potentials and silent periods in humans. Clin Neurophysiol 118:1204–1212
Tombu MN, Asplund CL, Dux PE, Godwin D, Martin JW, Marois R (2011) A unified attentional bottleneck in the human brain. Proc Natl Acad Sci 108:13426–13431
Vallesi A (2015) Dual-task costs in aging are predicted by formal education. Aging Clin Exp Res 27:1–6
Wilson SA, Lockwood RJ, Thickbroom GW, Mastaglia FL (1993) The muscle silent period following transcranial magnetic cortical stimulation. J Neurol Sci 114:216–222
Acknowledgments
This research was supported by an Endeavour Research Fellowship awarded to DC. The authors would like to thank B. Major for assistance with data collection.
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Appendix
Appendix
Were the following participant factors | Reported? | Controlled? |
---|---|---|
Age of subjects | ✓ | |
Gender of subjects | ✓ | |
Handedness of subjects | ✓ | |
Subjects prescribed medication | ✓ | |
Use of CNS active drugs (e.g. anti-convulsants) | ✓ | |
Presence of neurological/psychiatric disorders when studying healthy subjects | ✓ | |
Any medical conditions | ✓ | |
History of specific repetitive motor activity | ✗ | |
Were the following methodological factors | ||
Position and contact of EMG electrodes | ✓ | |
Amount of relaxation/contraction of target muscles | ✓ | |
Prior motor activity of the muscle to be tested | ✗ | |
Level of relaxation of muscles other than those being tested | ✓ | |
Coil type (size and geometry) | ✓ | |
Coil orientation | ✓ | |
Direction of induced current in the brain | ✓ | |
Coil location and stability (with or without a neuronavigation system) | ✓ | |
Type of stimulator used (e.g. brand) | ✓ | |
Stimulation intensity | ✓ | |
Pulse shape (monophasic or biphasic) | ✓ | |
Determination of optimal hotspot | ✓ | |
The time between MEP trials | ✓ | |
Time between days of testing | N/A | |
Subject attention (level of arousal) during testing | ✓ | |
Method for determining threshold (active/resting) | ✓ | |
Number of MEP measures made | ✓ | |
Paired pulse only: Intensity of test pulse | N/A | |
Paired pulse only: Intensity of conditioning pulse | N/A | |
Paired pulse only: Inter-stimulus interval | N/A | |
Were the following analytical factors | ||
Method for determining MEP size during analysis | ✓ | |
Size of unconditioned MEP | N/A |
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Corp, D.T., Rogers, M.A., Youssef, G.J. et al. The effect of dual-task difficulty on the inhibition of the motor cortex. Exp Brain Res 234, 443–452 (2016). https://doi.org/10.1007/s00221-015-4479-2
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DOI: https://doi.org/10.1007/s00221-015-4479-2