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Experimental Brain Research

, Volume 228, Issue 1, pp 9–24 | Cite as

Laterality affects spontaneous recovery of contralateral hand motor function following motor cortex injury in rhesus monkeys

  • Warren G. DarlingEmail author
  • Nicole Helle
  • Marc A. Pizzimenti
  • Diane L. Rotella
  • Stephanie M. Hynes
  • Jizhi Ge
  • Kimberly S. Stilwell-Morecraft
  • Robert J. Morecraft
Research Article

Abstract

The purpose of this study was to test whether brain laterality influences spontaneous recovery of hand motor function after controlled brain injuries to arm areas of M1 and lateral premotor cortex (LPMC) of the hemisphere contralateral to the preferred hand in rhesus monkeys. We hypothesized that monkeys with stronger hand preference would exhibit poorer recovery of skilled hand use after such brain injury. Degree of handedness was assessed using a standard dexterity board task in which subjects could use either hand to retrieve small food pellets. Fine hand/digit motor function was assessed using a modified dexterity board before and after the M1 and LPMC lesions in ten monkeys. We found a strong negative relationship between the degree of handedness and the recovery of manipulation skill, demonstrating that higher hand preference was associated with poorer recovery of hand fine motor function. We also observed that monkeys with larger lesions within M1 and LPMC had greater initial impairment of manipulation and poorer recovery of reaching skill. We conclude that monkeys with a stronger hand preference are likely to show poorer recovery of contralesional hand fine motor skill after isolated brain lesions affecting the lateral frontal motor areas. These data may be extended to suggest that humans who exhibit weak hand dominance, and perhaps individuals who use both hands for fine motor tasks, may have a more favorable potential for recovery after a unilateral stroke or brain injury affecting the lateral cortical motor areas than individuals with a high degree of hand dominance.

Keywords

Brain injury Hand Dexterity Hemispheric dominance 

Notes

Acknowledgments

This work was supported by National Institutes of Health Grant NS 046367.

References

  1. Anderson JS, Druzgal TJ, Froehlich A et al (2011) Decreased interhemispheric functional connectivity in autism. Cereb Cortex 21:1134–1146. doi: 10.1093/cercor/bhq190 PubMedCrossRefGoogle Scholar
  2. Darling WG, Peterson CR, Herrick JL, McNeal DW, Stilwell-Morecraft KS, Morecraft RJ (2006) Measurement of coordination of object manipulation in non-human primates. J Neurosci Methods 154:38–44. doi: 10.1016/j.jneumeth.2005.11.013 PubMedCrossRefGoogle Scholar
  3. 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 PubMedCrossRefGoogle Scholar
  4. Darling WG, Pizzimenti M, Hynes SM, Rotella, DL, Headley G, Ge J, Stilwell-Morecraft KS, McNeal DW, Solon-Cline KM, Morecraft RJ (2011) Volumetric effects of motor cortex injury on recovery of ispsilesional dexterous movements. Exp Neurol 231:56–71Google Scholar
  5. Dassonville P, Zhu XH, Uurbil K, Kim SG, Ashe J (1997) Functional activation in motor cortex reflects the direction and the degree of handedness. Proc Natl Acad Sci USA 94:14015–14018 [erratum appears in Proc Natl Acad Sci USA 1998 Sep 15;95(19):11499]PubMedCrossRefGoogle Scholar
  6. de Freitas PB, Krishnan V, Jaric S (2007) Force coordination in static manipulation tasks: effects of the change in direction and handedness. Exp Brain Res 183:487–497. doi: 10.1007/s00221-007-1064-3 PubMedCrossRefGoogle Scholar
  7. Dragovic M, Hammond G (2005) Handedness in schizophrenia: a quantitative review of evidence. Acta Psychiatr Scand 111:410–419. doi: 10.1111/j.1600-0447.2005.00519.x PubMedCrossRefGoogle Scholar
  8. Duff S, Sainburg R (2007) Lateralization of motor adaptation reveals independence in control of trajectory and steady-state position. Exp Brain Res 179:551PubMedCrossRefGoogle Scholar
  9. Harris JE, Eng JJ (2006) Individuals with the dominant hand affected following stroke demonstrate less impairment than those with the nondominant hand affected. Neurorehabil Neural Repair 20:380–389PubMedCrossRefGoogle Scholar
  10. Hopkins WD, Washburn DA, Rumbaugh DM (1989) Note on hand use in the manipulation of joysticks by rhesus monkeys (Macaca mulatta) and chimpanzees (Pan troglodytes). J Comp Psychol 103:91–94PubMedCrossRefGoogle Scholar
  11. Hopkins WD, Washburn DA, Berke L, Williams M (1992) Behavioral asymmetries of psychomotor performance in rhesus monkeys (Macaca mulatta): a dissociation between hand preference and skill. J Comp Psychol 106:392–397PubMedCrossRefGoogle Scholar
  12. Hughes CM, Franz EA (2007) Experience-dependent effects in unimanual and bimanual reaction time tasks in musicians. J Mot Behav 39:3–8. doi: 10.3200/JMBR.39.1.3-8 PubMedCrossRefGoogle Scholar
  13. Kaeser M, Brunet JF, Wyss A et al (2011) Autologous adult cortical cell transplantation enhances functional recovery following unilateral lesion of motor cortex in primates: a pilot study. Neurosurgery 68:1405–1416. doi: 10.1227/NEU.0b013e31820c02c0; discussion 1416–1407PubMedGoogle Scholar
  14. Kimura D (1977) Acquisition of a motor skill after left-hemisphere damage. Brain 100:527–542PubMedCrossRefGoogle Scholar
  15. Kimura D, Archibald Y (1974) Motor functions of the left hemisphere. Brain 97:337–350PubMedCrossRefGoogle Scholar
  16. Langan J, van Donkelaar P (2008) The influence of hand dominance on the response to a constraint-induced therapy program following stroke. Neurorehabil Neural Repair 22:298–304PubMedCrossRefGoogle Scholar
  17. Lehman RA (1978a) The handedness of rhesus monkeys—I. Distribution. Neuropsychologia 16:33–42PubMedCrossRefGoogle Scholar
  18. Lehman RA (1978b) The handedness of rhesus monkeys: II. Concurrent reaching. Cortex 14:190–196PubMedCrossRefGoogle Scholar
  19. Lehman RA (1980) The handedness of rhesus monkeys. III. Consistency within and across activities. Cortex 16:197–204PubMedCrossRefGoogle Scholar
  20. Liu Y, Rouiller EM (1999) Mechanisms of recovery of dexterity following unilateral lesion of the sensorimotor cortex in adult monkeys. Exp Brain Res 128:149–159PubMedCrossRefGoogle Scholar
  21. McCombe Waller S, Whitall J (2005) Hand dominance and side of stroke affect rehabilitation in chronic stroke. Clin Rehabil 19:544–551PubMedCrossRefGoogle Scholar
  22. 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 PubMedCrossRefGoogle Scholar
  23. 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
  24. Morecraft RJ, Herrick JL, Stilwell-Morecraft KS, Louie JL, Schroeder CM, Ottenbacher JG, Schoolfield MW (2002) Localization of arm representation in the corona radiata and internal capsule in the non-human primate. Brain 125:176–198Google Scholar
  25. 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
  26. 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 PubMedCrossRefGoogle Scholar
  27. 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
  28. Nagamoto-Combs K, McNeal DW, Morecraft RJ, Combs CK (2007) Prolonged microgliosis in the rhesus monkey central nervous system after traumatic brain injury. J Neurotrauma 24:1719–1742PubMedCrossRefGoogle Scholar
  29. Nagamoto-Combs K, Morecraft RJ, Darling WG, Combs CK (2010) Long-term gliosis and molecular changes in the cervical spinal cord of the rhesus monkey after traumatic brain injury. J Neurotrauma 27:565–585. doi: 10.1089/neu.2009.0966 PubMedCrossRefGoogle Scholar
  30. Nudo R, Jenkins W, Merzenich M, Prejean T, Grenda R (1992) Neurophysiological correlates of hand preference in primary motor cortex of adult squirrel monkeys. J Neurosci 12:2918–2947PubMedGoogle Scholar
  31. 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
  32. Pal PK, Hanajima R, Gunraj CA, Li JY, Wagle-Shukla A, Morgante F, Chen R (2005) Effect of low-frequency repetitive transcranial magnetic stimulation on interhemispheric inhibition. J Neurophysiol 94:1668–1675PubMedCrossRefGoogle Scholar
  33. 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
  34. Ridding MC, Brouwer B, Nordstrom MA (2000) Reduced interhemispheric inhibition in musicians. Exp Brain Res 133:249–253PubMedCrossRefGoogle Scholar
  35. Schaefer SY, Haaland KY, Sainburg RL (2007) Ipsilesional motor deficits following stroke reflect hemispheric specializations for movement control. Brain 130:2146–2158PubMedCrossRefGoogle Scholar
  36. Schaefer SY, Haaland KY, Sainburg RL (2009) Hemispheric specialization and functional impact of ipsilesional deficits in movement coordination and accuracy. Neuropsychologia 47(13):2953–2966PubMedCrossRefGoogle Scholar
  37. Schmahmann JD, Pandya DN (2006) Fiber pathways of the brain. Oxford University Press, New YorkCrossRefGoogle Scholar
  38. Schmitt V, Melchisedech S, Hammerschmidt K, Fischer J (2008) Hand preferences in Barbary macaques (Macaca sylvanus). Laterality 13:143–157. doi: 10.1080/13576500701757532 PubMedGoogle Scholar
  39. Spinozzi G, Lagana T, Truppa V (2007) Hand use by tufted capuchins (Cebus apella) to extract a small food item from a tube: digit movements, hand preference, and performance. Am J Primatol 69:336–352. doi: 10.1002/ajp.20352 PubMedCrossRefGoogle Scholar
  40. Toole JF, Flowers DL, Burdette JH, Absher JR (2007) A pianist’s recovery from stroke. Arch Neurol 64:1184–1188PubMedCrossRefGoogle Scholar
  41. Walton A, Scheib JL, McLean S, Zhang Z, Grondin R (2008) Motor memory preservation in aged monkeys mirrors that of aged humans on a similar task. Neurobiol Aging 29:1556–1562. doi: 10.1016/j.neurobiolaging.2007.03.016 PubMedCrossRefGoogle Scholar
  42. Wohrle JC, Haas F (2007) Hans von Bulow: creativity and neurological disease in a famous pianist and conductor. Front Neurol Neurosci 22:193–205. doi: 10.1159/0000102881 PubMedGoogle Scholar
  43. Zhang W, Sainburg RL, Zatsiorsky VM, Latash ML (2006) Hand dominance and multi-finger synergies. Neurosci Lett 409:200–204. doi: 10.1016/j.neulet.2006.09.048 PubMedCrossRefGoogle Scholar
  44. Zhao D, Hopkins WD, Li B (2012) Handedness in nature: first evidence on manual laterality on bimanual coordinated tube task in wild primates. Am J Phys Anthropol 148:36–44. doi: 10.1002/ajpa.22038 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Warren G. Darling
    • 1
    Email author
  • Nicole Helle
    • 1
  • Marc A. Pizzimenti
    • 2
  • Diane L. Rotella
    • 1
  • Stephanie M. Hynes
    • 1
  • Jizhi Ge
    • 3
  • Kimberly S. Stilwell-Morecraft
    • 3
  • Robert J. Morecraft
    • 3
  1. 1.Department of Health and Human Physiology, Motor Control LaboratoriesThe University of IowaIowa CityUSA
  2. 2.Department of Anatomy and Cell Biology, Carver College of MedicineThe University of IowaIowa CityUSA
  3. 3.Division of Basic Biomedical Sciences, Laboratory of Neurological Sciences, Sanford School of MedicineThe University of South DakotaVermillionUSA

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