Chimpanzee (Pan troglodytes) precentral corticospinal system asymmetry and handedness: A diffusion magnetic resonance imaging study

PLoS ONE

Volumn 5, Issue 9, 2010, Pages 1-13

  Li, Longchuan ^a   Preuss, Todd M ^a,b   Rilling, James K ^a,b   Hopkins, William D ^a,c   Glasser, Matthew F ^a   Kumar, Bhargav ^d   Nana, Roger ^a,d   Zhang, Xiaodong ^a   Hu, Xiaoping ^a,d  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AGNES SCOTT COLLEGE   (United States)

^d Emory University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHIMPANZEE; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; FEMALE; HANDEDNESS; HEMISPHERIC DOMINANCE; IN VIVO STUDY; LEFT HEMISPHERE; NONHUMAN; PYRAMIDAL TRACT; RIGHT HEMISPHERE; ANIMAL; PAN TROGLODYTES; PHYSIOLOGY; RADIOGRAPHY;

PAN; PAN TROGLODYTES;

ANIMALS; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; FUNCTIONAL LATERALITY; PAN TROGLODYTES; PYRAMIDAL TRACTS;

EID: 77958512047     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012886     Document Type: Article

References (99)

1. Corballis MC (1992) The lopsided brain: Evolution of the generative mind. New York: Oxford University Press.
2. McManus C (2002) Right hand, left hand: The origins of asymmetry in brains, bodies, atoms, and cultures. London: Weidenfeld & Nicolson.
3. Porac C, Coren S (1981) Lateral preferences and human behavior. New York: Springer.
4. Annett M (2002) Handedness and brain asymmetry: The right shift theory. Hove: Psychology Press.
5. Raymond M, Pontier D (2004) Is there geographical variation in human handedness? Laterality 9: 35-51.
6. Perelle IB, Ehrman L (1994) An international study of human handedness: The data. Behavior Genetics 24: 217-227.
7. Annett M (2004) Hand preference observed in large healthy samples: classification, norms and interpretations of increased non-right-handedness by the right shift theory. Br J Psychol 95: 339-353.
8. Annett M (1996) Laterality and types of dyslexia. Neurosci Biobehav Rev 20: 631-636.
9. Crow T (2004) Directional asymmetry is the key to the origin of modern Homo sapiens (the Broca-Annett axiom): A reply to Rogers' review of The Speciation of Modern Homo Sapiens. Laterality: Asymmetries of Body, Brain and Cognition 9: 233-242.
10. Warren JM (1980) Handedness and laterality in humans and other animals. Physiological Psychology 8: 351-359.
11. Bradshaw JL (1997) Human evolution: A neuropsychological perspective. In: Hove, editor. U.K.: Psychology Press.
12. Bradshaw JL, Rogers LJ (1993) The evolution of lateral asymmetries, language, tool use, and intellect. San Diego: Academic Press, Inc
13. Rogers LJ, Andrew JR (2002) Comparative vertebrate lateralization. Cambridge: Cambridge University Press.
14. Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: Advantages and disadvantages of cerebral lateralization. Behavioral and Brain Sciences 28: 574.
15. Hopkins WD (2006) Comparative and familial analysis of handedness in great apes. Psychological Bulletin 132: 538-559.
16. Hopkins WD (2007) Hemispheric specialization in chimpanzees: Evolution of hand and brain. In: Shackelford T, Keenan JP, Platek SM, editors. Evolutionary Cognitive Neuroscience. Boston: MIT Press. pp. 99-120.
17. Biro D, Inoue-Nakamura N, Tonooka R, Yamakoshi G, Sousa C, et al. (2003) Cultural innovation and transmission of tool use in wild chimpanzees: Evidence from field experiments. Animal Cognition 6: 213-223.
18. Byrne RW, Byrne JM (1991) Hand preferences in the skilled gathering tasks of mountain gorillas (Gorilla gorilla berengei). Cortex 27: 521-536.
19. Corp N, Byrne RW (2004) Sex difference in chimpanzee handedness. American Journal of Physical Anthropology 123: 62-68.
20. Humle T, Matsuzawa T (2009) Laterality in hand use across four tool use behaviors among the wild chimpanzees of Bossou, Guinea, West Africa. American Journal of Primatology 71: 40-48.
21. Lonsdorf EV, Hopkins WD (2005) Wild chimpanzees show population level handedness for tool use. Proceedings of the National Academy of Sciences 102: 12634-12638.
22. Marchant LF, McGrew WC (2007) Ant fishing by wild chimpanzees is not lateralised Primates 48: 22-26.
23. Hopkins WD (1995) Hand preferences for a coordinated bimanual task in 110 chimpanzees (Pan troglodytes): cross-sectional analysis. J Comp Psychol 109: 291-297.
24. Hopkins WD, Fernandez-Carriba S, Wesley MJ, Hostetter A, Pilcher D, et al. (2001) The use of bouts and frequencies in the evaluation of hand preferences for a coordinated bimanual task in chimpanzees (Pan troglodytes): an empirical study comparing two different indices of laterality. J Comp Psychol 115: 294-299.
25. Hopkins WD, Cantalupo C (2003) Does variation in sample size explain individual differences in hand preferences of chimpanzees (Pan troglodytes)? An empirical study and reply to Palmer (2002). Am J Phys Anthropol 121: 378-381;author reply 382-374.
26. Hopkins WD, Cantalupo C, Freeman H, Russell J, Kachin M, et al. (2005) Chimpanzees are right-handed when recording bouts of hand use. Laterality 10: 121-130.
27. Amunts K, Schlaug G, Schleicher A, Steinmetz H, Dabringhaus A, et al. (1996) Asymmetry in the human motor cortex and handedness. Neuroimage 4: 216-222.
28. Amunts K, Jancke L, Mohlberg H, Steinmetz H, Zilles K (2000) Interhemispheric asymmetry of the human motor cortex related to handedness and gender. Neuropsychologia 38: 304-312.
29. Buchel C, Raedler T, Sommer M, Sach M, Weiller C, et al. (2004) White matter asymmetry in the human brain: a diffusion tensor MRI study. Cereb Cortex 14: 945-951.
30. Hammond G (2002) Correlates of human handedness in primary motor cortex: a review and hypothesis. Neuroscience and Biobehavioral Reviews 26: 285-292.
31. Basser PJ (1995) Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed 8: 333-344.
32. Basser PJ, Jones DK (2002) Diffusion-tensor MRI: theory, experimental design and data analysis - a technical review. NMR Biomed 15: 456-467.
33. Basser PJ, Mattiello J, LeBihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103: 247-254.
34. Jones DK (2008) Studying connections in the living human brain with diffusion MRI. Cortex 44: 936-952.
35. Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G (1996) Diffusion tensor MR imaging of the human brain. Radiology 201: 637-648.
36. Conturo TE, Lori NF, Cull TS, Akbudak E, Snyder AZ, et al. (1999) Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci U S A 96: 10422-10427.
37. Jones DK, Simmons A, Williams SC, Horsfield MA (1999) Non-invasive assessment of axonal fiber connectivity in the human brain via diffusion tensor MRI. Magn Reson Med 42: 37-41.
38. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44: 625-632.
39. Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? Neuroimage 34: 144-155.
40. Kumar A, Juhasz C, Asano E, Sundaram SK, Makki MI, et al. (2009) Diffusion tensor imaging study of the cortical origin and course of the corticospinal tract in healthy children. AJNR Am J Neuroradiol 30: 1963-1970.
41. Guye M, Parker GJ, Symms M, Boulby P, Wheeler-Kingshott CA, et al. (2003) Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortex in vivo. Neuroimage 19: 1349-1360.
42. Park HJ, Westin CF, Kubicki M, Maier SE, Niznikiewicz M, et al. (2004) White matter hemisphere asymmetries in healthy subjects and in schizophrenia: a diffusion tensor MRI study. Neuroimage 23: 213-223.
43. Westerhausen R, Huster RJ, Kreuder F, Wittling W, Schweiger E (2007) Corticospinal tract asymmetries at the level of the internal capsule: is there an association with handedness? Neuroimage 37: 379-386.
44. Dubois J, Benders M, Lazeyras F, Borradori-Tolsa C, Leuchter RH, et al. (2010) Structural asymmetries of perisylvian regions in the preterm newborn. Neuroimage 52: 32-42.
45. Hopkins WD, Cantalupo C (2004) Handedness in chimpanzees (Pan troglodytes) is associated with asymmetries of the primary motor cortex but not with homologous language areas. Behav Neurosci 118: 1176-1183.
46. Dadda M, Cantalupo C, Hopkins WD (2006) Further evidence of an association between handedness and neuroanatomical asymmetries in the primary motor cortex of chimpanzees (Pan troglodytes). Neuropsychologia 44: 2582-2586.
47. Hopkins WD, Russell JL, Cantalupo C (2007) Neuroanatomical correlates of handedness for tool use in chimpanzees (Pan troglodytes): Implication for theories on the evolution of language. Psychological Science 18: 971-977.
48. Taglialatela JP, Cantalupo C, Hopkins WD (2006) Gesture handedness predicts asymmetry in the chimpanzee inferior frontal gyrus. NeuroReport 17: 923-927.
49. Alexander AL, Tsuruda JS, Parker DL (1997) Elimination of eddy current artifacts in diffusion-weighted echo-planar images: the use of bipolar gradients. Magn Reson Med 38: 1016-1021.
50. Andersson JL, Skare S, Ashburner J (2003) How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. Neuroimage 20: 870-888.
51. Hopkins WD, Wesley MJ, Izard MK, Hook M, Schapiro SJ (2004) Chimpanzees are predominantly right-handed: Replication in three colonies of apes. Behavioral Neuroscience 118: 659-663.
52. Phillips K, Sherwood CS (2005) Primary motor cortex asymmetry correlates with handedness in capcuhin monkeys (Cebus apella). Behavioral Neuroscience 119: 1701-1704.
53. Hopkins WD, Taglialatela JP, Dunham L, Pierre P (2007) Behavioral and neuroanatomical correlates of white matter asymmetries in chimpanzees (Pan troglodytes). Eur J Neurosci 25: 2565-2570.
54. Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17: 143-155.
55. Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 20: 45-57.
56. Smith MS, Brady JM (1997) SUSAN - A new approach to low level image processing. International Journal of Computer Vision 23: 45-78.
57. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, et al. (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31: 1487-1505.
58. Smith SM, Johansen-Berg H, Jenkinson M, Rueckert D, Nichols TE, et al. (2007) Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nat Protoc 2: 499-503.
59. Kochunov P, Thompson PM, Lancaster JL, Bartzokis G, Smith S, et al. (2007) Relationship between white matter fractional anisotropy and other indices of cerebral health in normal aging: tract-based spatial statistics study of aging. Neuroimage 35: 478-487.
60. Anjari M, Srinivasan L, Allsop JM, Hajnal JV, Rutherford MA, et al. (2007) Diffusion tensor imaging with tract-based spatial statistics reveals local white matter abnormalities in preterm infants. Neuroimage 35: 1021-1027.
61. Richards T, Stevenson J, Crouch J, Johnson LC, Maravilla K, et al. (2008) Tract-based spatial statistics of diffusion tensor imaging in adults with dyslexia. AJNR Am J Neuroradiol 29: 1134-1139.
62. Della Nave R, Ginestroni A, Tessa C, Salvatore E, De Grandis D, et al. (2008) Brain white matter damage in SCA1 and SCA2. An in vivo study using voxel-based morphometry, histogram analysis of mean diffusivity and tract-based spatial statistics. Neuroimage 43: 10-19.
63. Martin RF, Bowden DM (1996) A stereotaxic template atlas of the macaque brain for digital imaging and quantitative neuroanatomy. Neuroimage 4: 119-150.
64. Davidoff RA (1990) The pyramidal tract. Neurology 40: 332-339.
65. Ebeling U, Reulen HJ (1992) Subcortical topography and proportions of the pyramidal tract. Acta Neurochir (Wien) 118: 164-171.
66. Morecraft RJ, Herrick JL, Stilwell-Morecraft KS, Louie JL, Schroeder CM, et al. (2002) Localization of arm representation in the corona radiata and internal capsule in the non-human primate. Brain 125: 176-198.
67. Rademacher J, Burgel U, Geyer S, Schormann T, Schleicher A, et al. (2001) Variability and asymmetry in the human precentral motor system. A cytoarchitectonic and myeloarchitectonic brain mapping study. Brain 124: 2232-2258.
68. Sherwood CC, Broadfield DC, Holloway RL, Gannon PJ, Hof PR (2003) Variability of Broca's area homologue in African great apes: implications for language evolution. Anat Rec A Discov Mol Cell Evol Biol 271: 276-285.
69. Bailey P, Bonin Gv, McCulloch WS (1950) The isocortex of the chimpanzee. Urbana, IL: Univ. of Illionois Press.
70. Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44: 83-98.
71. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15: 1-25.
72. Kertesz A, Geschwind N (1971) Patterns of pyramidal decussation and their relationship to handedness. Arch Neurol 24: 326-332.
73. Burgel U, Amunts K, Hoemke L, Mohlberg H, Gilsbach JM, et al. (2006) White matter fiber tracts of the human brain: three-dimensional mapping at microscopic resolution, topography and intersubject variability. Neuroimage 29: 1092-1105.
74. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, et al. (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17: 1429-1436.
75. Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, et al. (2003) Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 20: 1714-1722.
76. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, et al. (2005) Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26: 132-140.
77. Li L, Coles CD, Lynch ME, Hu X (2009) Voxelwise and skeleton-based region of interest analysis of fetal alcohol syndrome and fetal alcohol spectrum disorders in young adults. Hum Brain Mapp 30: 3265-3274.
78. Foundas AL, Hong K, Leonard CM, Heilman KM (1998) Hand preference and magnetic resonance imaging asymmetries of the central sulcus. Neuropsychiatry Neuropsychol Behav Neurol 11: 65-71.
79. White LE, Lucas G, Richards A, Purves D (1994) Cerebral asymmetry and handedness. Nature 368: 197-198.
80. Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 15: 435-455.
81. Kroliczak G, Frey SH (2009) A common network in the left cerebral hemisphere represents planning of tool use pantomimes and familiar intransitive gestures at the hand-independent level. Cereb Cortex 19: 2396-2410.
82. Frey SH, Funnell MG, Gerry VE, Gazzaniga MS (2005) A dissociation between the representation of tool-use skills and hand dominance: insights from left- and right-handed callosotomy patients. J Cogn Neurosci 17: 262-272.
83. Boesch C, Head J, Robbins MM (2009) Complex tool sets for honey extraction among chimpanzees in Loango National Park, Gabon. J Hum Evol 56: 560-569.
84. Bril B, Dietrich G, Foucart J, Fuwa K, Hirata S (2009) Tool use as a way to assess cognition: how do captive chimpanzees handle the weight of the hammer when cracking a nut? Anim Cogn 12: 217-235.
85. Toga AW, Thompson PM (2003) Mapping brain asymmetry. Nat Rev Neurosci 4: 37-48.
86. Thatcher RW, Walker RA, Giudice S (1987) Human cerebral hemispheres develop at different rates and ages. Science 236: 1110-1113.
87. Herve PY, Leonard G, Perron M, Pike B, Pitiot A, et al. (2009) Handedness, motor skills and maturation of the corticospinal tract in the adolescent brain. Hum Brain Mapp 30: 3151-3162.
88. Stieltjes B, Kaufmann WE, van Zijl PC, Fredericksen K, Pearlson GD, et al. (2001) Diffusion tensor imaging and axonal tracking in the human brainstem. Neuroimage 14: 723-735.
89. Okada T, Mikuni N, Miki Y, Kikuta K, Urayama S, et al. (2006) Corticospinal tract localization: integration of diffusion-tensor tractography at 3-T MR imaging with intraoperative white matter stimulation mapping-preliminary results. Radiology 240: 849-857.
90. Reich DS, Smith SA, Jones CK, Zackowski KM, van Zijl PC, et al. (2006) Quantitative characterization of the corticospinal tract at 3T. AJNR Am J Neuroradiol 27: 2168-2178.
91. Habas C, Cabanis EA (2007) Anatomical parcellation of the brainstem and cerebellar white matter: a preliminary probabilistic tractography study at 3 T. Neuroradiology 49: 849-863.
92. Dubois J, Hertz-Pannier L, Cachia A, Mangin JF, Le Bihan D, et al. (2009) Structural asymmetries in the infant language and sensori-motor networks. Cereb Cortex 19: 414-423.
93. Schmahmann JD, Rosene DL, Pandya DN (2004) Motor projections to the basis pontis in rhesus monkey. J Comp Neurol 478: 248-268.
94. Nieuwenhuys R, Voogd J, Huijzen C (2007) The human central nervous system (the fourth edition)
95. Nagae-Poetscher LM, Jiang H, Wakana S, Golay X, van Zijl PC, et al. (2004) High-resolution diffusion tensor imaging of the brain stem at 3 T. AJNR Am J Neuroradiol 25: 1325-1330.
96. Ciccarelli O, Behrens TE, Altmann DR, Orrell RW, Howard RS, et al. (2006) Probabilistic diffusion tractography: a potential tool to assess the rate of disease progression in amyotrophic lateral sclerosis. Brain 129: 1859-1871.
97. Abe O, Yamada H, Masutani Y, Aoki S, Kunimatsu A, et al. (2004) Amyotrophic lateral sclerosis: diffusion tensor tractography and voxel-based analysis. NMR Biomed 17: 411-416.
98. Gong G, Jiang T, Zhu C, Zang Y, He Y, et al. (2005) Side and handedness effects on the cingulum from diffusion tensor imaging. Neuroreport 16: 1701-1705.
99. Parker GJ, Luzzi S, Alexander DC, Wheeler-Kingshott CA, Ciccarelli O, et al. (2005) Lateralization of ventral and dorsal auditory-language pathways in the human brain. Neuroimage 24: 656-666.