Laterality Affects Spontaneous Recovery of Contralateral Hand Motor Function Following Motor Cortex Injury in Rhesus Monkeys

Overview

Journal Exp Brain Res

Specialty Neurology

Date 2013 May 9

PMID 23652723

Citations 7

Authors

Warren G Darling

Nicole Helle

Marc A Pizzimenti

Diane L Rotella

Stephanie M Hynes

Jizhi Ge

Kimberly S Stilwell-Morecraft

Robert J Morecraft

Affiliations

Soon will be listed here.

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.

Citing Articles

A computational model based on corticospinal functional MRI revealed asymmetrically organized motor corticospinal networks in humans.

Takasawa E, Abe M, Chikuda H, Hanakawa T Commun Biol. 2022; 5(1):664.

PMID: 35790815 PMC: 9256686. DOI: 10.1038/s42003-022-03615-2.

Changes in ipsilesional hand motor function differ after unilateral injury to frontal versus frontoparietal cortices in Macaca mulatta.

Darling W, Pizzimenti M, Rotella D, Ge J, Stilwell-Morecraft K, Morecraft R Exp Brain Res. 2019; 238(1):205-220.

PMID: 31834452 DOI: 10.1007/s00221-019-05690-0.

Terminal organization of the corticospinal projection from the lateral premotor cortex to the cervical enlargement (C5-T1) in rhesus monkey.

Morecraft R, Ge J, Stilwell-Morecraft K, Rotella D, Pizzimenti M, Darling W J Comp Neurol. 2019; 527(16):2761-2789.

PMID: 31032921 PMC: 6721988. DOI: 10.1002/cne.24706.

Sensorimotor cortex injury effects on recovery of contralesional dexterous movements in Macaca mulatta.

Darling W, Pizzimenti M, Rotella D, Hynes S, Ge J, Stilwell-Morecraft K Exp Neurol. 2016; 281:37-52.

PMID: 27091225 PMC: 4898655. DOI: 10.1016/j.expneurol.2016.04.004.

Recruitment of the prefrontal cortex and cerebellum in Parkinsonian rats following skilled aerobic exercise.

Wang Z, Guo Y, Myers K, Heintz R, Holschneider D Neurobiol Dis. 2015; 77:71-87.

PMID: 25747184 PMC: 4402279. DOI: 10.1016/j.nbd.2015.02.020.

References

Morecraft R, Stilwell-Morecraft K, Cipolloni P, Ge J, McNeal D, Pandya D . Cytoarchitecture and cortical connections of the anterior cingulate and adjacent somatomotor fields in the rhesus monkey. Brain Res Bull. 2012; 87(4-5):457-97. PMC: 3295893. DOI: 10.1016/j.brainresbull.2011.12.005. View

Hopkins W, WASHBURN D, Rumbaugh D . Note on hand use in the manipulation of joysticks by rhesus monkeys (Macaca mulatta) and chimpanzees (Pan troglodytes). J Comp Psychol. 1989; 103(1):91-4. DOI: 10.1037/0735-7036.103.1.91. View

Lehman R . The handedness of rhesus monkeys. III. Consistency within and across activities. Cortex. 1980; 16(2):197-204. DOI: 10.1016/s0010-9452(80)80055-4. View

Darling W, Pizzimenti M, Rotella D, Peterson C, Hynes S, Ge J . Volumetric effects of motor cortex injury on recovery of dexterous movements. Exp Neurol. 2009; 220(1):90-108. PMC: 2778269. DOI: 10.1016/j.expneurol.2009.07.034. View

Ridding M, Brouwer B, Nordstrom M . Reduced interhemispheric inhibition in musicians. Exp Brain Res. 2000; 133(2):249-53. DOI: 10.1007/s002210000428. View

Langan J, van Donkelaar P . The influence of hand dominance on the response to a constraint-induced therapy program following stroke. Neurorehabil Neural Repair. 2007; 22(3):298-304. DOI: 10.1177/1545968307307123. View

Schaefer S, Haaland K, Sainburg R . Hemispheric specialization and functional impact of ipsilesional deficits in movement coordination and accuracy. Neuropsychologia. 2009; 47(13):2953-66. PMC: 2752301. DOI: 10.1016/j.neuropsychologia.2009.06.025. View

Nagamoto-Combs K, Morecraft R, Darling W, Combs C . Long-term gliosis and molecular changes in the cervical spinal cord of the rhesus monkey after traumatic brain injury. J Neurotrauma. 2009; 27(3):565-85. PMC: 2867631. DOI: 10.1089/neu.2009.0966. View

Lehman R . The handedness of rhesus monkeys--I. Distribution. Neuropsychologia. 1978; 16(1):33-42. DOI: 10.1016/0028-3932(78)90040-4. View

10.

Murata Y, Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M . Effects of motor training on the recovery of manual dexterity after primary motor cortex lesion in macaque monkeys. J Neurophysiol. 2007; 99(2):773-86. DOI: 10.1152/jn.01001.2007. View

11.

Kaeser M, Brunet J, Wyss A, Belhaj-Saif A, Liu Y, Hamadjida A . Autologous adult cortical cell transplantation enhances functional recovery following unilateral lesion of motor cortex in primates: a pilot study. Neurosurgery. 2011; 68(5):1405-16. DOI: 10.1227/NEU.0b013e31820c02c0. View

12.

Toole J, Lynn Flowers D, Burdette J, Absher J . A pianist's recovery from stroke. Arch Neurol. 2007; 64(8):1184-8. DOI: 10.1001/archneur.64.8.1184. View

13.

Darling W, Peterson C, Herrick J, McNeal D, Stilwell-Morecraft K, Morecraft R . Measurement of coordination of object manipulation in non-human primates. J Neurosci Methods. 2006; 154(1-2):38-44. DOI: 10.1016/j.jneumeth.2005.11.013. View

14.

Spinozzi G, Lagana T, Truppa V . 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. 2006; 69(3):336-52. DOI: 10.1002/ajp.20352. View

15.

Harris J, Eng J . Individuals with the dominant hand affected following stroke demonstrate less impairment than those with the nondominant hand affected. Neurorehabil Neural Repair. 2006; 20(3):380-9. PMC: 3432641. DOI: 10.1177/1545968305284528. View

16.

Nagamoto-Combs K, McNeal D, Morecraft R, Combs C . Prolonged microgliosis in the rhesus monkey central nervous system after traumatic brain injury. J Neurotrauma. 2007; 24(11):1719-42. DOI: 10.1089/neu.2007.0377. View

17.

Walton A, Scheib J, McLean S, Zhang Z, Grondin R . Motor memory preservation in aged monkeys mirrors that of aged humans on a similar task. Neurobiol Aging. 2007; 29(10):1556-62. DOI: 10.1016/j.neurobiolaging.2007.03.016. View

18.

Dragovic M, Hammond G . Handedness in schizophrenia: a quantitative review of evidence. Acta Psychiatr Scand. 2005; 111(6):410-9. DOI: 10.1111/j.1600-0447.2005.00519.x. View

19.

Pizzimenti M, Darling W, Rotella D, McNeal D, Herrick J, Ge J . Measurement of reaching kinematics and prehensile dexterity in nonhuman primates. J Neurophysiol. 2007; 98(2):1015-29. DOI: 10.1152/jn.00354.2007. View

20.

Waller S, Whitall J . Hand dominance and side of stroke affect rehabilitation in chronic stroke. Clin Rehabil. 2005; 19(5):544-51. DOI: 10.1191/0269215505cr829oa. View