Simultaneous brain–cervical cord fMRI reveals intrinsic spinal cord plasticity during motor sequence learning

PLoS Biology

Volumn 13, Issue 6, 2015, Pages 1-25

  Vahdat, Shahabeddin ^a,b   Lungu, Ovidiu ^a,b   Cohen Adad, Julien ^b,c   Marchand Pauvert, Veronique ^d   Benali, Habib ^b,d   Doyon, Julien ^a,b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b SensoriMotor Rehabilitation Research Team of the Canadian Institute for Health Research   (Canada)

^c ÉCOLE POLYTECHNIQUE DE MONTRÉAL   (Canada)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BRAIN; BRAIN FUNCTION; CEREBELLUM; CERVICAL SPINAL CORD; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MOTOR PERFORMANCE; MOTOR SEQUENCE LEARNING; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROMODULATION; NORMAL HUMAN; SENSORIMOTOR CORTEX; SPINAL CORD PLASTICITY; YOUNG ADULT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; SPINAL CORD;

BRAIN; FEMALE; HEALTHY VOLUNTEERS; HUMANS; LEARNING; MAGNETIC RESONANCE IMAGING; MALE; MOTOR SKILLS; SPINAL CORD; YOUNG ADULT;

EID: 84934763093     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002186     Document Type: Article

References (57)

1. Doyon J, Benali H (2005) Reorganization and plasticity in the adult brain during learning of motor skills. Curr Opin Neurobiol 15: 161-167. PMID: 15831397
2. Doyon J, Bellec P, Amsel R, Penhune V, Monchi O, et al. (2009) Contributions of the basal ganglia and functionally related brain structures to motor learning. Behavioural brain research 199: 61-75. doi: 10. 1016/j. bbr. 2008. 11. 012 PMID: 19061920
3. Seidler RD (2010) Neural correlates of motor learning, transfer of learning, and learning to learn. Exerc Sport Sci Rev 38: 3-9. doi: 10. 1097/JES. 0b013e3181c5cce7 PMID: 20016293
4. Dayan E, Cohen LG (2011) Neuroplasticity subserving motor skill learning. Neuron 72: 443-454. doi: 10. 1016/j. neuron. 2011. 10. 008 PMID: 22078504
5. Grau JW (2013) Learning from the spinal cord: How the study of spinal cord plasticity informs our view of learning. Neurobiol Learn Mem 108: 155-171. doi: 10. 1016/j. nlm. 2013. 08. 003 PMID: 23973905
6. Wolpaw JR (2010) What can the spinal cord teach us about learning and memory? Neuroscientist 16: 532-549. doi: 10. 1177/1073858410368314 PMID: 20889964
7. Rossignol S, Frigon A (2011) Recovery of locomotion after spinal cord injury: some facts and mechanisms. Annu Rev Neurosci 34: 413-440. doi: 10. 1146/annurev-neuro-061010-113746 PMID: 21469957
8. Wang Y, Pillai S, Wolpaw JR, Chen XY (2006) Motor learning changes GABAergic terminals on spinal motoneurons in normal rats. Eur J Neurosci 23: 141-150. PMID: 16420424
9. Wolpaw JR, Lee CL (1989) Memory traces in primate spinal cord produced by operant conditioning of H-reflex. J Neurophysiol 61: 563-572. PMID: 2709100
10. Nielsen J, Crone C, Hultborn H (1993) H-reflexes are smaller in dancers from The Royal Danish Ballet than in well-trained athletes. Eur J Appl Physiol Occup Physiol 66: 116-121. PMID: 8472692
11. Casabona A, Polizzi MC, Perciavalle V (1990) Differences in H-reflex between athletes trained for explosive contractions and non-trained subjects. Eur J Appl Physiol Occup Physiol 61: 26-32. PMID: 2289495
12. Wolpert DM, Diedrichsen J, Flanagan JR (2011) Principles of sensorimotor learning. Nat Rev Neurosci 12: 739-751. doi: 10. 1038/nrn3112 PMID: 22033537
13. Scott SH (2012) The computational and neural basis of voluntary motor control and planning. Trends Cogn Sci 16: 541-549. doi: 10. 1016/j. tics. 2012. 09. 008 PMID: 23031541
14. Lungu O, Frigon A, Piche M, Rainville P, Rossignol S, et al. (2010) Changes in spinal reflex excitability associated with motor sequence learning. J Neurophysiol 103: 2675-2683. doi: 10. 1152/jn. 00006. 2010 PMID: 20237314
15. Meunier S, Kwon J, Russmann H, Ravindran S, Mazzocchio R, et al. (2007) Spinal use-dependent plasticity of synaptic transmission in humans after a single cycling session. J Physiol 579: 375-388. PMID: 17170047
16. Perez MA, Lundbye-Jensen J, Nielsen JB (2006) Changes in corticospinal drive to spinal motoneurones following visuo-motor skill learning in humans. J Physiol 573: 843-855. PMID: 16581867
17. Albouy G, King BR, Maquet P, Doyon J (2013) Hippocampus and striatum: dynamics and interaction during acquisition and sleep-related motor sequence memory consolidation. Hippocampus 23: 985-1004. doi: 10. 1002/hipo. 22183 PMID: 23929594
18. Orban P, Peigneux P, Lungu O, Albouy G, Breton E, et al. (2010) The multifaceted nature of the relationship between performance and brain activity in motor sequence learning. Neuroimage 49: 694-702. doi: 10. 1016/j. neuroimage. 2009. 08. 055 PMID: 19732838
19. Marrelec G, Krainik A, Duffau H, Pelegrini-Issac M, Lehericy S, et al. (2006) Partial correlation for functional brain interactivity investigation in functional MRI. Neuroimage 32: 228-237. PMID: 16777436
20. Vahdat S, Darainy M, Ostry DJ (2014) Structure of plasticity in human sensory and motor networks due to perceptual learning. J Neurosci 34: 2451-2463. doi: 10. 1523/JNEUROSCI. 4291-13. 2014 PMID: 24523536
21. He SQ, Dum RP, Strick PL (1993) Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J Neurosci 13: 952-980. PMID: 7680069
22. He SQ, Dum RP, Strick PL (1995) Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. J Neurosci 15: 3284-3306. PMID: 7538558
23. Bentivoglio M (1982) The organization of the direct cerebellospinal projections. Prog Brain Res 57: 279-291. PMID: 6296920
24. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, et al. (1997) Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6: 218-229. PMID: 9344826
25. Verma T, Cohen-Adad J (2014) Effect of respiration on the B field in the human spinal cord at 3T. Magn Reson Med 72: 1629-1636. doi: 10. 1002/mrm. 25075 PMID: 24390654
26. Fratini M, Moraschi M, Maraviglia B, Giove F (2014) On the impact of physiological noise in spinal cord functional MRI. J Magn Reson Imaging 40: 770-777. doi: 10. 1002/jmri. 24467 PMID: 24925698
27. Cohen-Adad J, Mareyam A, Keil B, Polimeni JR, Wald LL (2011) 32-channel RF coil optimized for brain and cervical spinal cord at 3 T. Magn Reson Med 66: 1198-1208. doi: 10. 1002/mrm. 22906 PMID: 21433068
28. Finsterbusch J, Sprenger C, Buchel C (2013) Combined T2*-weighted measurements of the human brain and cervical spinal cord with a dynamic shim update. Neuroimage 79: 153-161. doi: 10. 1016/j. neuroimage. 2013. 04. 021 PMID: 23603283
29. Eippert F, Finsterbusch J, Bingel U, Buchel C (2009) Direct evidence for spinal cord involvement in placebo analgesia. Science 326: 404. doi: 10. 1126/science. 1180142 PMID: 19833962
30. Sprenger C, Eippert F, Finsterbusch J, Bingel U, Rose M, et al. (2012) Attention modulates spinal cord responses to pain. Curr Biol 22: 1019-1022. doi: 10. 1016/j. cub. 2012. 04. 006 PMID: 22608507
31. Vahdat S, Darainy M, Milner TE, Ostry DJ (2011) Functionally specific changes in resting-state sensorimotor networks after motor learning. J Neurosci 31: 16907-16915. doi: 10. 1523/JNEUROSCI. 2737- 11. 2011 PMID: 22114261
32. Barry RL, Smith SA, Dula AN, Gore JC (2014) Resting state functional connectivity in the human spinal cord. Elife 3: e02812. doi: 10. 7554/eLife. 02812 PMID: 25097248
33. Kong Y, Eippert F, Beckmann CF, Andersson J, Finsterbusch J, et al. (2014) Intrinsically organized resting state networks in the human spinal cord. Proc Natl Acad Sci U S A 111: 18067-18072. doi: 10. 1073/pnas. 1414293111 PMID: 25472845
34. Yoshizawa T, Nose T, Moore GJ, Sillerud LO (1996) Functional magnetic resonance imaging of motor activation in the human cervical spinal cord. Neuroimage 4: 174-182. PMID: 9345507
35. Stroman PW, Nance PW, Ryner LN (1999) BOLD MRI of the human cervical spinal cord at 3 tesla. Magn Reson Med 42: 571-576. PMID: 10467302
36. Madi S, Flanders AE, Vinitski S, Herbison GJ, Nissanov J (2001) Functional MR imaging of the human cervical spinal cord. AJNR Am J Neuroradiol 22: 1768-1774. PMID: 11673177
37. Cadotte DW, Stroman PW, Mikulis D, Fehlings MG (2012) A systematic review of spinal fMRI research: outlining the elements of experimental design. J Neurosurg Spine 17: 102-118. doi: 10. 3171/2012. 5. AOSPINE1278 PMID: 22985377
38. Maieron M, Iannetti GD, Bodurka J, Tracey I, Bandettini PA, et al. (2007) Functional responses in the human spinal cord during willed motor actions: evidence for side- and rate-dependent activity. J Neurosci 27: 4182-4190. PMID: 17428996
39. Stroman PW, Tomanek B, Krause V, Frankenstein UN, Malisza KL (2003) Functional magnetic resonance imaging of the human brain based on signal enhancement by extravascular protons (SEEP fMRI). Magn Reson Med 49: 433-439. PMID: 12594745
40. Franklin DW, Burdet E, Tee KP, Osu R, Chew CM, et al. (2008) CNS learns stable, accurate, and efficient movements using a simple algorithm. J Neurosci 28: 11165-11173. doi: 10. 1523/JNEUROSCI. 3099-08. 2008 PMID: 18971459
41. Gao F, Latash ML, Zatsiorsky VM (2005) Control of finger force direction in the flexion-extension plane. Exp Brain Res 161: 307-315. PMID: 15726342
42. Milner TE, Dhaliwal SS (2002) Activation of intrinsic and extrinsic finger muscles in relation to the fingertip force vector. Exp Brain Res 146: 197-204. PMID: 12195521
43. Wymbs NF, Bassett DS, Mucha PJ, Porter MA, Grafton ST (2012) Differential recruitment of the sensorimotor putamen and frontoparietal cortex during motor chunking in humans. Neuron 74: 936-946. doi: 10. 1016/j. neuron. 2012. 03. 038 PMID: 22681696
44. Tresch MC, Saltiel P, Bizzi E (1999) The construction of movement by the spinal cord. Nat Neurosci 2: 162-167. PMID: 10195201
45. Wulf G, McNevin N, Shea CH (2001) The automaticity of complex motor skill learning as a function of attentional focus. Q J Exp Psychol A 54: 1143-1154. PMID: 11765737
46. Mars RB, Bestmann S, Rothwell JC, Haggard P (2007) Effects of motor preparation and spatial attention on corticospinal excitability in a delayed-response paradigm. Exp Brain Res 182: 125-129. PMID: 17634929
47. Jankowska E (2001) Spinal interneuronal systems: identification, multifunctional character and reconfigurations in mammals. J Physiol 533: 31-40. PMID: 11351010
48. Hagbarth KE, Kerr DI (1954) Central influences on spinal afferent conduction. J Neurophysiol 17: 295-307. PMID: 13163716
49. Hagains CE, Senapati AK, Huntington PJ, He JW, Peng YB (2011) Inhibition of spinal cord dorsal horn neuronal activity by electrical stimulation of the cerebellar cortex. J Neurophysiol 106: 2515-2522. doi: 10. 1152/jn. 00719. 2010 PMID: 21832034
50. Del Olmo MF, Cheeran B, Koch G, Rothwell JC (2007) Role of the cerebellum in externally paced rhythmic finger movements. J Neurophysiol 98: 145-152. PMID: 17460103
51. Rao SM, Mayer AR, Harrington DL (2001) The evolution of brain activation during temporal processing. Nat Neurosci 4: 317-323. PMID: 11224550
52. Smith AM (1996) Does the cerebellum learn strategies for the optimal time-varying control of joint stiffness? Behavioral and Brain Sciences 19: 399-410.
53. Karni A, Meyer G, Jezzard P, Adams MM, Turner R, et al. (1995) Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377: 155-158. PMID: 7675082
54. Cohen-Adad J, Gauthier CJ, Brooks JC, Slessarev M, Han J, et al. (2010) BOLD signal responses to controlled hypercapnia in human spinal cord. Neuroimage 50: 1074-1084. doi: 10. 1016/j. neuroimage. 2009. 12. 122 PMID: 20060914
55. Beckmann CF, Jenkinson M, Smith SM (2003) General multilevel linear modeling for group analysis in FMRI. Neuroimage 20: 1052-1063. PMID: 14568475
56. Xie G, Piche M, Khoshnejad M, Perlbarg V, Chen JI, et al. (2012) Reduction of physiological noise with independent component analysis improves the detection of nociceptive responses with fMRI of the human spinal cord. Neuroimage 63: 245-252. doi: 10. 1016/j. neuroimage. 2012. 06. 057 PMID: 22776463
57. Hansen PC, Jensen TK, Rodriguez G (2007) An adaptive pruning algorithm for the discrete L-curve criterion. Journal of Computational and Applied Mathematics 198: 483-492.