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Experimental Brain Research

, Volume 232, Issue 12, pp 3929–3938 | Cite as

Recovery of precision grasping after motor cortex lesion does not require forced use of the impaired hand in macaca mulatta

  • Warren G. DarlingEmail author
  • Robert J. Morecraft
  • Diane L. Rotella
  • Marc A. Pizzimenti
  • Jizhi Ge
  • Kimberly S. Stilwell-Morecraft
  • Hongyu Zhang
  • Hesham Soliman
  • Dave Seecharan
  • Ian Edwards
  • David McNeal
  • Randolph J. Nudo
  • Paul Cheney
Research Article

Abstract

We investigated recovery of precision grasping of small objects between the index finger and thumb of the impaired hand without forced use after surgically placed lesions to the hand/arm areas of M1 and M1 + lateral premotor cortex in two monkeys. The unilateral lesions were contralateral to the monkey’s preferred hand, which was established in prelesion testing as the hand used most often to acquire raisins in a foraging board (FB) task in which the monkey was free to use either hand to acquire treats. The lesions initially produced a clear paresis of the contralesional hand and use of only the ipsilesional hand to acquire raisins in the FB task. However, beginning about 3 weeks after the lesion both monkeys spontaneously began using the impaired contralesional hand in the FB task and increased use of that hand over the next few tests. Moreover, the monkeys clearly used precision grasp to acquire the raisins in a similar manner to prelesion performances, although grasp durations were longer. Although the monkeys used the contralesional hand more often than the ipsilesional hand in some postlesion testing sessions, they did not recover to use the hand as often as in prelesion testing when the preferred hand was used almost exclusively. These findings suggest that recovery of fine hand/digit motor function after localized damage to the lateral frontal motor areas in rhesus monkeys does not require forced use of the impaired hand.

Keywords

Finger Grip Dexterity 

Notes

Acknowledgments

Supported by U.S. National Institutes of Health Grants NS064054, NS046367 and NS30853.

Supplementary material

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Supplementary material 1 (WMV 130 kb)
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Supplementary material 2 (WMV 184 kb)

Supplementary material 3 (WMV 192 kb)

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Supplementary material 4 (WMV 138 kb)

References

  1. Alstermark B, Pettersson LG, Nishimura Y, Yoshino-Saito K, Tsuboi F, Takahashi M, Isa T (2011) Motor command for precision grip in the macaque monkey can be mediated by spinal interneurons. J Neurophysiol 106:122–126. doi: 10.1152/jn.00089.2011 PubMedCrossRefGoogle Scholar
  2. Bradnam LV, Stinear CM, Byblow WD (2013) Ipsilateral motor pathways after stroke: implications for non-invasive brain stimulation. Front Hum Neurosci 7:184. doi: 10.3389/fnhum.2013.00184 PubMedCentralPubMedCrossRefGoogle Scholar
  3. Cheney PD, Hill-Karrer J, Belhaj-Saif A, McKiernan BJ, Park MC, Marcario JK (2000) Cortical motor areas and their properties: implications for neuroprosthetics. Prog Brain Res 128:135–160PubMedCrossRefGoogle Scholar
  4. Darling WG, Pizzimenti MA, Rotella DL et al (2009) Volumetric effects of motor cortex injury on recovery of dexterous movements. Exp Neurol 220:90–108. doi: 10.1016/j.expneurol.2009.07.034 PubMedCentralPubMedCrossRefGoogle Scholar
  5. Darling WG, Pizzimenti MA, Rotella DL et al (2010) Minimal forced use without constraint stimulates spontaneous use of the impaired upper extremity following motor cortex injury. Exp Brain Res 202:529–542. doi: 10.1007/s00221-010-2157-y PubMedCentralPubMedCrossRefGoogle Scholar
  6. Darling WG, Pizzimenti MA, Hynes SM et al (2011a) Volumetric effects of motor cortex injury on recovery of ipsilesional dexterous movements. Exp Neurol 231:56–71. doi: 10.1016/j.expneurol.2011.05.015 PubMedCentralPubMedCrossRefGoogle Scholar
  7. Darling WG, Pizzimenti MA, Morecraft RJ (2011b) Functional recovery following motor cortex lesions in non-human primates: experimental implications for human stroke patients. J Integr Neurosci 10:353–384. doi: 10.1142/S0219635211002737 PubMedCentralPubMedCrossRefGoogle Scholar
  8. Frost SB, Barbay S, Friel KM, Plautz EJ, Nudo RJ (2003) Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. J Neurophysiol 89:3205–3214. doi: 10.1152/jn.01143.2002 PubMedCrossRefGoogle Scholar
  9. Glees P, Cole J (1950) Recovery of skilled motor functions after small repeated lesions of motor cortex in macaque. J Neurophysiol 13:137–148Google Scholar
  10. Graham Brown T, Sherrington CS (1913) Note on the functions of the cortex cerebri. J Physiol (Lond) 46(suppl):xxiiGoogle Scholar
  11. Higo N (2014) Effects of rehabilitative training on recovery of hand motor function: a review of animal studies. Neurosci Res 78:9–15. doi: 10.1016/j.neures.2013.09.008 PubMedCrossRefGoogle Scholar
  12. Kinoshita M, Matsui R, Kato S et al (2012) Genetic dissection of the circuit for hand dexterity in primates. Nature 487:235–238. doi: 10.1038/nature11206 PubMedCrossRefGoogle Scholar
  13. Lemon RN (2008) Descending pathways in motor control. Annu Rev Neurosci 31:195–218. doi: 10.1146/annurev.neuro.31.060407.125547 PubMedCrossRefGoogle Scholar
  14. Lemon RN, Baker SN, Davis JA, Kirkwood PA, Maier MA, Yang HS (1998) The importance of the cortico-motoneuronal system for control of grasp. Novartis Found Symp 218:202–215 (discussion 215–208)PubMedGoogle Scholar
  15. Leyton ASF, Sherrington CS (1917) Observations on the excitable cortex of the chimpanzee, orangutan and gorilla. Exp Physiol 11:135–222Google Scholar
  16. McNeal DW, Darling WG, Ge J et al (2010) Selective long-term reorganization of the corticospinal projection from the supplementary motor cortex following recovery from lateral motor cortex injury. J Comp Neurol 518:586–621. doi: 10.1002/cne.22218 PubMedCentralPubMedCrossRefGoogle Scholar
  17. Moore TL, Killiany RJ, Pessina MA, Moss MB, Finklestein SP, Rosene DL (2012) Recovery from ischemia in the middle-aged brain: a nonhuman primate model. Neurobiology of Aging 33:619e619–619e624. doi: 10.1016/j.neurobiolaging.2011.02.005 CrossRefGoogle Scholar
  18. Morecraft RJ, Geula C, Mesulam MM (1992) Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey. J Comp Neurol 323:341–358PubMedCrossRefGoogle Scholar
  19. Morecraft RJ, Cipolloni PB, Stilwell-Morecraft KS, Gedney MT, Pandya DN (2004) Cytoarchitecture and cortical connections of the posterior cingulate and adjacent somatosensory fields in the rhesus monkey. J Comp Neurol 469:37–69PubMedCrossRefGoogle Scholar
  20. Morecraft RJ, Stilwell-Morecraft KS, Cipolloni PB, Ge J, McNeal DW, Pandya DN (2012) Cytoarchitecture and cortical connections of the anterior cingulate and adjacent somatomotor fields in the rhesus monkey. Brain Res Bull 87:457–497. doi: 10.1016/j.brainresbull.2011.12.005 PubMedCentralPubMedCrossRefGoogle Scholar
  21. Morris DM, Taub E (2001) Constraint-induced therapy approach to restoring function after neurological injury. Top Stroke Rehabil 8:16–30PubMedCrossRefGoogle Scholar
  22. Murata Y, Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M, Yamane S (2008) Effects of motor training on the recovery of manual dexterity after primary motor cortex lesion in macaque monkeys. J Neurophysiol 99:773–786. doi: 10.1152/jn.01001.2007 PubMedCrossRefGoogle Scholar
  23. Nudo RJ, Milliken GW (1996) Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J Neurophysiol 75:2144–2149PubMedGoogle Scholar
  24. Nudo RJ, Wise BM, SiFuentes F, Milliken GW (1996) Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 272:1791–1794PubMedCrossRefGoogle Scholar
  25. Passingham RE, Perry VH, Wilkinson F (1983) The long-term effects of removal of sensorimotor cortex in infant and adult rhesus monkeys. Brain 106(Pt 3):675–705PubMedCrossRefGoogle Scholar
  26. Pizzimenti MA, Darling WG, Rotella DL et al (2007) Measurement of reaching kinematics and prehensile dexterity in nonhuman primates. J Neurophysiol 98:1015–1029. doi: 10.1152/jn.00354.2007 PubMedCrossRefGoogle Scholar
  27. Rathelot JA, Strick PL (2009) Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proc Natl Acad Sci USA 106:918–923. doi: 10.1073/pnas.0808362106 PubMedCentralPubMedCrossRefGoogle Scholar
  28. Sasaki S, Isa T, Pettersson LG et al (2004) Dexterous finger movements in primate without monosynaptic corticomotoneuronal excitation. J Neurophysiol 92:3142–3147. doi: 10.1152/jn.00342.2004 PubMedCrossRefGoogle Scholar
  29. Schmahmann JD, Pandya DN (2006) Fiber pathways of the brain. Oxford University Press, New YorkCrossRefGoogle Scholar
  30. Smania N, Gandolfi M, Paolucci S et al (2012) Reduced-intensity modified constraint-induced movement therapy versus conventional therapy for upper extremity rehabilitation after stroke: a multicenter trial. Neurorehabil Neural Repair 26:1035–1045. doi: 10.1177/1545968312446003 PubMedCrossRefGoogle Scholar
  31. Taub E, Miller NE, Novack TA et al (1993) Technique to improve chronic motor deficit after stroke. Arch Phys Med Rehabil 74:347–354PubMedGoogle Scholar
  32. Taub E, Crago JE, Burgio LD, Groomes TE, Cook EW 3rd, DeLuca SC, Miller NE (1994) An operant approach to rehabilitation medicine: overcoming learned nonuse by shaping. J Exp Anal Behav 61:281–293PubMedCentralPubMedCrossRefGoogle Scholar
  33. Taub E, Uswatte G, Mark VW, Morris DM (2006) The learned nonuse phenomenon: implications for rehabilitation. Eura Medicophys 42:241–256PubMedGoogle Scholar
  34. Treger I, Aidinof L, Lehrer H, Kalichman L (2012) Modified constraint-induced movement therapy improved upper limb function in subacute poststroke patients: a small-scale clinical trial. Top Stroke Rehabil 19:287–293. doi: 10.1310/tsr1904-287 PubMedCrossRefGoogle Scholar
  35. Wolf SL, Winstein CJ, Miller JP et al (2006) Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial. JAMA 296:2095–2104. doi: 10.1001/jama.296.17.2095 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2014

Authors and Affiliations

  • Warren G. Darling
    • 1
    Email author
  • Robert J. Morecraft
    • 2
  • Diane L. Rotella
    • 1
  • Marc A. Pizzimenti
    • 1
    • 3
  • Jizhi Ge
    • 2
  • Kimberly S. Stilwell-Morecraft
    • 2
  • Hongyu Zhang
    • 4
  • Hesham Soliman
    • 5
  • Dave Seecharan
    • 5
  • Ian Edwards
    • 4
  • David McNeal
    • 6
  • Randolph J. Nudo
    • 4
    • 6
  • Paul Cheney
    • 4
  1. 1.Department of Health and Human PhysiologyUniversity of IowaIowa CityUSA
  2. 2.Division of Basic Biomedical SciencesUniversity of South Dakota School of MedicineVermillionUSA
  3. 3.Department of Anatomy and Cell BiologyUniversity of IowaIowa CityUSA
  4. 4.Department of Molecular and Integrative PhysiologyUniversity of Kansas Medical CenterKansas CityUSA
  5. 5.Department of NeurosurgeryUniversity of Kansas Medical CenterKansas CityUSA
  6. 6.Landon Center on AgingUniversity of Kansas Medical CenterKansas CityUSA

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