Ann Rehabil Med.  2012 Aug;36(4):501-511. 10.5535/arm.2012.36.4.501.

Prediction of Motor Function Recovery after Subcortical Stroke: Case Series of Activation PET and TMS Studies

Affiliations
  • 1Department of Rehabilitation Medicine, Seoul Metropolitan Government-Seoul National University Boramae Medical Center, Seoul 156-707, Korea.
  • 2Department of Nuclear Medicine, Seoul Metropolitan Government-Seoul National University Boramae Medical Center, Seoul 156-707, Korea.
  • 3Department of Nuclear Medicine, Seoul National University College of Medicine, Seoul National University Bundang Hospital, Seongnam 463-707, Korea.
  • 4Department of Rehabilitation Medicine, Seoul National University College of Medicine, Seoul National University Bundang Hospital, Seongnam 463-707, Korea. njpaik@snu.ac.kr

Abstract


OBJECTIVE
To examine whether the pattern of brain activation induced by a motor task and the motor responses to transcranial magnetic stimulation (TMS) have prognostic implications for motor recovery after stroke. METHOD: Ten patients with first-ever subcortical stroke (55.7+/-17.3 years, 5 ischemic and 5 hemorrhagic) underwent 2 FDG PET studies under different conditions (1: rest, 2: activation with a specific motor task) at 37.7+/-25.2 days after stroke. The regions showing more than a 10% increase in glucose metabolism on subtraction images during activation and rest were considered to be significantly activated. Cortical excitability of intracortical inhibition (ICI) and intracortical facilitation (ICF) were assessed using the TMS from both abductor pollicis brevis muscles within 7 days of PET scans. Recovery of motor function was assessed at the point of the neurological plateau.
RESULTS
The presence of a motor response at the plegic site to TMS and normal intracortical inhibition, and facilitation patterns in the unaffected hemisphere were found to be related to good recovery. An association between an ipsilesional activation on PET and good motor recovery was also observed, but this was significantly weaker than that between TMS measured cortical excitability and motor recovery.
CONCLUSION
Integrity of the ipsilesional corticospinal pathway, normalized contralesional intracortical excitability, and task-related activation in the ipsilesional hemisphere were found to predict post-stroke motor recovery significantly.

Keyword

Stroke; Motor recovery; PET; Transcranial magnetic stimulation; Activation pattern

MeSH Terms

Brain
Glucose
Humans
Muscles
Positron-Emission Tomography
Recovery of Function
Stroke
Transcranial Magnetic Stimulation
Glucose

Figure

  • Fig. 1 A patient in a good recovery group (Patient 4). (A) Brain CT showed a hemorrhagic lesion in the right thalamus. (B) During the motor task, activation was observed in the cerebellum and perilesional motor cortex (arrow) on her FDG-PET. (C) Normal ICI and ICF response patterns were observed in bilateral motor cortices on the paired pulse TMS. ICI: Intracortical inhibition, ICF: Intracortical facilitation, ISI: Interstimulus interval, ms: Milliseconds.

  • Fig. 2 A patient in a fair recovery group (Patient 3). (A) Brain MRI showed an acute infarct in the left corona radiata. (B) During the motor task, activation occurred in the contralateral motor cortex, the cerebellum, the perilesional area, bilateral frontal cortices and thalamus. (C) No MEP was observed in the affected APB, but normal ICI and ICF patterns were observed in the unaffected side. ICI: Intracortical inhibition, ICF: Intracortical facilitation, ISI: Interstimulus interval, ms: Milliseconds.


Reference

1. Karni A, Meyer G, Jezzard P, Adams MM, Turner R, Ungerleider LG. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature. 1995; 377:155–158. PMID: 7675082.
Article
2. Mattay VS, Weinberger DR. Organization of the human motor system as studied by functional magnetic resonance imaging. Eur J Radiol. 1999; 30:105–114. PMID: 10401591.
Article
3. Calautti C, Leroy F, Guincestre JY, Marié RM, Baron JC. Sequential activation brain mapping after subcortical stroke: changes in hemispheric balance and recovery. Neuroreport. 2001; 12:3883–3886. PMID: 11742203.
Article
4. Loubinoux I, Carel C, Pariente J, Dechaumont S, Albucher JF, Marque P, Manelfe C, Chollet F. Correlation between cerebral reorganization and motor recovery after subcortical infarcts. Neuroimage. 2003; 20:2166–2180. PMID: 14683720.
Article
5. Brouwer BJ, Schryburt-Brown K. Hand function and motor cortical output poststroke: are they related? Arch Phys Med Rehabil. 2006; 87:627–634. PMID: 16635624.
Article
6. Rossini PM, Pauri F. Neuromagnetic integrated methods tracking human brain mechanisms of sensorimotor areas 'plastic' reorganisation. Brain Res Brain Res Rev. 2000; 33:131–154. PMID: 11011062.
Article
7. Cramer SC, Nelles G, Benson RR, Kaplan JD, Parker RA, Kwong KK, Kennedy DN, Finklestein SP, Rosen BR. A functional MRI study of subjects recovered from hemiparetic stroke. Stroke. 1997; 28:2518–2527. PMID: 9412643.
Article
8. Seitz RJ, Höflich P, Binkofski F, Tellmann L, Herzog H, Freund HJ. Role of the premotor cortex in recovery from middle cerebral artery infarction. Arch Neurol. 1998; 55:1081–1088. PMID: 9708958.
Article
9. Johansen-Berg H, Dawes H, Guy C, Smith SM, Wade DT, Matthews PM. Correlation between motor improvements and altered fMRI activity after rehabilitative therapy. Brain. 2002; 125:2731–2742. PMID: 12429600.
10. Cramer SC. Functional imaging in stroke recovery. Stroke. 2004; 35:2695–2698. PMID: 15388899.
Article
11. Marshall RS, Perera GM, Lazar RM, Krakauer JW, Constantine RC, DeLaPaz RL. Evolution of cortical activation during recovery from corticospinal tract infarction. Stroke. 2000; 31:656–661. PMID: 10700500.
Article
12. Bütefisch CM, Netz J, Wessling M, Seitz RJ, Hömberg V. Remote changes in cortical excitability after stroke. Brain. 2003; 126:470–481. PMID: 12538413.
13. Zemke AC, Heagerty PJ, Lee C, Cramer SC. Motor cortex organization after stroke is related to side of stroke and level of recovery. Stroke. 2003; 34:e23–e28. PMID: 12677024.
Article
14. Herholz K, Westwood S, Haense C, Dunn G. Evaluation of a calibrated (18)F-FDG PET score as a biomarker for progression in Alzheimer disease and mild cognitive impairment. J Nucl Med. 2011; 52:1218–1226. PMID: 21764801.
Article
15. Bashir S, Mizrahi I, Weaver K, Fregni F, Pascual-Leone A. Assessment and modulation of neural plasticity in rehabilitation with transcranial magnetic stimulation. PM R. 2010; 2:S253–S268. PMID: 21172687.
Article
16. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971; 9:97–113. PMID: 5146491.
Article
17. Maquet P, Dive D, Salmon E, von Frenckel R, Franck G. Reproducibility of cerebral glucose utilization measured by PET and the [18F]-2-fluoro-2-deoxy-d-glucose method in resting, healthy human subjects. Eur J Nucl Med. 1990; 16:267–273. PMID: 2351175.
Article
18. Tombari D, Loubinoux I, Pariente J, Gerdelat A, Albucher JF, Tardy J, Cassol E, Chollet F. A longitudinal fMRI study: in recovering and then in clinically stable sub-cortical stroke patients. Neuroimage. 2004; 23:827–839. PMID: 15528083.
Article
19. Heiss WD, Kessler J, Thiel A, Ghaemi M, Karbe H. Differential capacity of left and right hemispheric areas for compensation of poststroke aphasia. Ann Neurol. 1999; 45:430–438. PMID: 10211466.
Article
20. Cao Y, Vikingstad EM, George KP, Johnson AF, Welch KM. Cortical language activation in stroke patients recovering from aphasia with functional MRI. Stroke. 1999; 30:2331–2340. PMID: 10548667.
Article
21. Carey LM, Abbott DF, Egan GF, Bernhardt J, Donnan GA. Motor impairment and recovery in the upper limb after stroke: behavioral and neuroanatomical correlates. Stroke. 2005; 36:625–629. PMID: 15677574.
22. Richards LG, Stewart KC, Woodbury ML, Senesac C, Cauraugh JH. Movement-dependent stroke recovery: a systematic review and meta-analysis of TMS and fMRI evidence. Neuropsychologia. 2008; 46:3–11. PMID: 17904594.
Article
23. Triggs WJ, Calvanio R, Levine M. Transcranial magnetic stimulation reveals a hemispheric asymmetry correlate of intermanual differences in motor performance. Neuropsychologia. 1997; 35:1355–1363. PMID: 9347481.
Article
24. Hendricks HT, Pasman JW, van Limbeek J, Zwarts MJ. Motor evoked potentials of the lower extremity in predicting motor recovery and ambulation after stroke: a cohort study. Arch Phys Med Rehabil. 2003; 84:1373–1379. PMID: 13680577.
25. van Kuijk AA, Pasman JW, Geurts AC, Hendricks HT. How salient is the silent period? The role of the silent period in the prognosis of upper extremity motor recovery after severe stroke. J Clin Neurophysiol. 2005; 22:10–24. PMID: 15689709.
Article
26. Seitz RJ, Höflich P, Binkofski F, Tellmann L, Herzog H, Freund HJ. Role of the premotor cortex in recovery from middle cerebral artery infarction. Arch Neurol. 1998; 55:1081–1088. PMID: 9708958.
Article
27. Stinear C. Prediction of recovery of motor function after stroke. Lancet Neurol. 2010; 9:1228–1232. PMID: 21035399.
Article
28. Coupar F, Pollock A, Rowe P, Weir C, Langhorne P. Predictors of upper limb recovery after stroke: a systematic review and meta-analysis. Clin Rehabil. 2012; 26:291–313. PMID: 22023891.
Article
29. Pennisi G, Rapisarda G, Bella R, Calabrese V, Maertens De Noordhout A, Delwaide PJ. Absence of response to early transcranial magnetic stimulation in ischemic stroke patients: prognostic value for hand motor recovery. Stroke. 1999; 30:2666–2670. PMID: 10582994.
30. Hendricks HT, Pasman JW, Merx JL, van Limbeek J, Zwarts MJ. Analysis of recovery processes after stroke by means of transcranial magnetic stimulation. J Clin Neurophysiol. 2003; 20:188–195. PMID: 12881665.
Article
31. van Kuijk AA, Pasman JW, Hendricks HT, Zwarts MJ, Geurts AC. Predicting hand motor recovery in severe stroke: the role of motor evoked potentials in relation to early clinical assessment. Neurorehabil Neural Repair. 2009; 23:45–51. PMID: 18794218.
Article
32. Cicinelli P, Pasqualetti P, Zaccagnini M, Traversa R, Oliveri M, Rossini PM. Interhemispheric asymmetries of motor cortex excitability in the postacute stroke stage: a paired-pulse transcranial magnetic stimulation study. Stroke. 2003; 34:2653–2658. PMID: 14551397.
33. Talelli P, Greenwood RJ, Rothwell JC. Arm function after stroke: neurophysiological correlates and recovery mechanisms assessed by transcranial magnetic stimulation. Clin Neurophysiol. 2006; 117:1641–1659. PMID: 16595189.
Article
34. Lioumis P, Mustanoja S, Bikmullina R, Vitikainen AM, Kičić D, Salonen O, Tatlisumak T, Kaste M, Forss N, Mäkelä JP. Probing modifications of cortical excitability during stroke recovery with navigated transcranial magnetic stimulation. Top Stroke Rehabil. 2012; 19:182–192. PMID: 22436366.
Article
Full Text Links
  • ARM
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr