Distinction between hand dominance and hand preference in primates: A behavioral investigation of manual dexterity in nonhuman primates (macaques) and human subjects

Brain and Behavior

Volumn 3, Issue 5, 2013, Pages 575-595

  Chatagny, Pauline ^a   Badoud, Simon ^a   Kaeser, Mélanie ^a   Gindrat, Anne Dominique ^a   Savidan, Julie ^a   Fregosi, Michela ^a   Moret, Véronique ^a   Roulin, Christine ^a   Schmidlin, Eric ^a   Rouiller, Eric M ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

Bimanual coordination; Handedness; Intermanual difference; Motor performance; Precision grip

Indexed keywords

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; FEMALE; FUNCTIONAL ASSESSMENT; HAND FUNCTION; HAND GRIP; HAND PREFERENCE; HUMAN; LEFT HANDEDNESS; MACACA FASCICULARIS; MOTOR PERFORMANCE; NONHUMAN; PRIORITY JOURNAL; RIGHT HANDEDNESS; SCORING SYSTEM; SELF EVALUATION; SEX DIFFERENCE; SPECIES DIFFERENCE; STIMULUS RESPONSE; TASK PERFORMANCE;

EID: 84893466535     PISSN: None     EISSN: 21623279     Source Type: Journal    
DOI: 10.1002/brb3.160     Document Type: Article

References (85)

1. Brinkman, C. 1984. Supplementary motor area of the monkey's cerebral cortex: short- and long-term deficits after unilateral ablation and the effects of subsequent callosal section. J. Neurosci. 4:918-929.
2. Brinkman, J., and H. G. J. M. Kuypers 1973. Cerebral control of contralateral and ipsilateral arm, hand and finger movements in the split-brain rhesus monkey. Brain 96:653-674.
3. Brinkman, C., and M. Smithson 2007. Determinants of hand preference in monkeys (M. fascicularis): birth to weaning. Aust. J. Psychol. 59(Suppl. 1):21.
4. Chapelain, A., P. Bec, and C. Blois-Heulin 2006. Manual laterality in Campbell's Monkeys (Cercopithecus c. campbelli) in spontaneous and experimental actions. Behav. Brain Res. 173:237-245.
5. Coren, S., and C. Porac 1977. Fifty centuries of right-handedness: the historical record. Science 198:631-632.
6. Dadda, M., C. Cantalupo, and W. D. Hopkins 2006. Further evidence of an association between handedness and neuroanatomical asymmetries in the primary motor cortex of chimpanzees (Pan troglodytes). Neuropsychologia 44:2582-2586.
7. Dassonville, P., X. H. Zhu, K. Uurbil, S. G. Kim, and J. Ashe 1997. Functional activation in motor cortex reflects the direction and the degree of handedness. Proc. Natl. Acad. Sci. USA 94:14015-14018.
8. Fagot, J., and J. Vauclair 1988. Handedness and manual specialization in the baboon. Neuropsychologia 26:795-804.
9. Fagot, J., and J. Vauclair 1991. Manual laterality in nonhuman primates: a distinction between handedness and manual specialization. Psychol. Bull. 109:76-89.
10. Fooden, J. 2006. Comparative review of fascicularis-group species of macaques (Primates: Macaca). Fieldiana Zool. 107:1-44.
11. Forrester, G. S., C. Quaresmini, D. A. Leavens, D. Mareschal, and M. S. C. Thomas 2013. Human handedness: an inherited evolutionary trait. Behav. Brain Res. 237:200-2006.
12. Freund, P., E. Schmidlin, T. Wannier, J. Bloch, A. Mir, M. E. Schwab, et al. 2009. Anti-Nogo-A antibody treatment promotes recovery of manual dexterity after unilateral cervical lesion in adult primates-re-examination and extension of behavioral data. Eur. J. Neurosci. 29:983-996.
13. Hanbury, D. B., K. D. Edens, D. A. Bunch, C. E. Legg, and S. L. Watson 2010. Multiple measures of laterality in Garnett's bushbaby (Otolemur garnettii). Am. J. Primatol. 72:206-216.
14. Hopkins, W. D. 1995. Hand preferences for a coordinated bimanual task in 110 chimpanzees (Pan troglodytes): cross-sectional analysis. J. Comp. Psychol. 109:291-297.
15. Hopkins, W. D. 2004. Laterality in maternal cradling and infant positional biases: implications for the development and evolution of hand preferences in nonhuman primates. Int. J. Primatol. 25:1243-1265.
16. Hopkins, W. D. 2006. Comparative and familial analysis of handedness in great apes. Psychol. Bull. 132:538-559.
17. Hopkins, W. D., and C. Cantalupo 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.
18. Hopkins, W. D., and C. Cantalupo 2005. Individual and setting differences in the hand preferences of chimpanzees (Pan troglodytes): a critical analysis and some alternative explanations. Laterality 10:65-80.
19. Hopkins, W. D., and D. L. Pilcher 2001. Neuroanatomical localization of the motor hand area with magnetic resonance imaging: the left hemisphere is larger in great apes. Behav. Neurosci. 115:1159-1164.
20. Hopkins, W. D., and D. M. Rabinowitz 1997. Manual specialisation and tool use in captive chimpanzees (Pan troglodytes): the effect of unimanual and bimanual strategies on hand preference. Laterality 2:267-277.
21. Hopkins, W. D., D. A. Washburn, and D. M. Rumbaugh 1989. Note on hand use in the manipulation of joysticks by rhesus monkeys (Macaca mulatta) and chimpanzees (Pan troglodytes). J. Comp. Psychol. 103:91-94.
22. Hopkins, W. D., D. A. Washburn, L. Berke, and M. Williams 1992. Behavioral asymmetries of psychomotor performance in rhesus monkeys (Macaca mulatta): a dissociation between hand preference and skill. J. Comp. Psychol. 106:392-397.
23. Hopkins, W. D., C. Cantalupo, M. J. Wesley, A. B. Hostetter, and D. L. Pilcher 2002. Grip morphology and hand use in chimpanzees (Pan troglodytes): evidence of a left hemisphere specialization in motor skill. J. Exp. Psychol. Gen. 131:412-423.
24. Hopkins, W. D., M. Hook, S. Braccini, and S. J. Schapiro 2003. Population-level right handedness for a coordinated bimanual task in chimpanzees: replication and extension in a second colony of apes. Int. J. Primatol. 24:677-689.
25. Hopkins, W. D., M. J. Wesley, M. K. Izard, M. Hook, and S. J. Schapiro 2004. Chimpanzees (Pan troglodytes) are predominantly right-handed: replication in three populations of apes. Behav. Neurosci. 118:659-663.
26. Hopkins, W. D., J. L. Russell, C. Cantalupo, H. Freeman, and S. J. Schapiro 2005. Factors influencing the prevalence and handedness for throwing in captive chimpanzees (Pan troglodytes). J. Comp. Psychol. 119:363-370.
27. Hopkins, W. D., J. P. Taglialatela, J. L. Russell, T. M. Nir, and J. Schaeffer 2010. Cortical representation of lateralized grasping in chimpanzees (Pan troglodytes): a combined MRI and PET study. PLoS One 5:e13383.
28. Hopkins, W. D., K. A. Phillips, A. Bania, S. E. Calcutt, M. Gardner, J. Russell, et al. 2011. Hand preferences for coordinated bimanual actions in 777 great apes: implications for the evolution of handedness in hominins. J. Hum. Evol. 60:605-611.
29. Kaeser, M., A. F. Wyss, S. Bashir, A. Hamadjida, Y. Liu, J. Bloch, et al. 2010. Effects of unilateral motor cortex lesion on ipsilesional hand's reach and grasp performance in monkeys: relationship with recovery in the contralesional hand. J. Neurophysiol. 103:1630-1645.
30. Kaeser, M., J. F. Brunet, A. Wyss, A. Belhaj-Saif, Y. Liu, A. Hamadjida, 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.
31. Kaeser, M., T. Wannier, J. F. Brunet, A. Wyss, J. Bloch, and E. M. Rouiller 2013. Representation of motor habit in a sequence of repetitive reach and grasp movements performed by macaque monkeys: evidence for a contribution of the dorsolateral prefrontal cortex. Cortex 49:1404-1419.
32. Kastner-Koller, U., P. Deimann, and J. Bruckner 2007. Assessing handedness in pre-schoolers: construction and initial validation of a hand preference test for 4-6 year olds. Psychol. Sci. 49:239-254.
33. Kazennikov, O., U. Wicki, M. Corboz, B. Hyland, A. Palmeri, E. M. Rouiller, et al. 1994. Temporal structure of a bimanual goal-directed movement sequence in monkeys. Eur. J. Neurosci. 6:203-210.
34. Kermadi, I., Y. Liu, A. Tempini, E. Calciati, and E. M. Rouiller 1998. Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination. Somatosens. Mot. Res. 15:287-308.
35. Kermadi, I., Y. Liu, and E. M. Rouiller 2000. Do bimanual motor actions involve the dorsal premotor (PMd), cingulate (CMA) and posterior parietal (PPC) cortices? Comparison with primary and supplementary motor cortical areas. Somatosens. Mot. Res. 17:255-271.
36. Kimura, D. 2000. Sex and cognition. MIT Press, Cambridge, MA.
37. Kinoshita, M. 1998. Do monkeys choose the more skillful hand in manual problem-solving? Percept. Mot. Skills 87:83-89.
38. Lacreuse, A., and D. M. Fragaszy 1997. Manual exploratory procedures and asymmetries for a haptic search task: a comparison between capuchins (Cebus apella) and humans. Laterality 2:247-266.
39. Lacreuse, A., L. A. Parr, H. M. Smith, and W. D. Hopkins 1999. Hand preferences for a ahptic task in chimpanzees (Pan troglodytes). Int. J. Primatol. 20:867-881.
40. Lehman, R. A. 1978a. The handedness of rhesus monkeys: I. Distribution. Neuropsychologia 16:33-42.
41. Lehman, R. A. 1978b. The handedness of rhesus monkeys: II. Concurrent reaching. Cortex 14:190-196.
42. Lehman, R. A. 1980a. The handedness of rhesus monkeys: III. Consistency within and across activities. Cortex 16:197-204.
43. Lehman, R. A. 1980b. Distribution and changes in strength of hand preferences of cynomolgus monkeys. Brain Behav. Evol. 17:209-217.
44. Lehman, R. A. 1989. Hand preferences of rhesus monkeys on differing tasks. Neuropsychologia 27:1193-1196.
45. Leliveld, L. M., M. Scheumann, and E. Zimmermann 2008. Manual lateralization in early primates: a comparison of two mouse lemur species. Am. J. Phys. Anthropol. 137:156-163.
46. Lemon, R. N. 1993. Cortical control of the primate hand. Exp. Physiol. 78:263-301.
47. Lemon, R. N. 2008. Descending pathways in motor control. Annu. Rev. Neurosci. 31:195-218.
48. Liu, Y., and E. M. Rouiller 1999. Mechanisms of recovery of dexterity following unilateral lesion of the sensorimotor cortex in adult monkeys. Exp. Brain Res. 128:149-159.
49. MacManus, I. C. 2009. Brief handedness questionnaire. Available at http://www.ucl.ac.uk/medical-education/other-studies/laterality/laterality-questionnaires/BriefHandednessQuestionnaire2009.pdf (accessed 22 July 2013).
50. MacNeilage, P. F., M. G. Studert-Kennedy, and B. Lindblom 1987. Primate handedness reconsidered. Behav. Brain Sci. 10:247-303.
51. Mark, R. F., and R. W. Sperry 1968. Bimanual coordination in monkeys. Exp. Neurol. 21:92-104.
52. Masataka, N. 1989. Population-level asymetry of hand preference in lemurs. Behaviour 110:244-247.
53. Meguerditchian, A., J. Donnot, S. Molesti, R. Francioly, and J. Vauclair 2012. Sex difference in squirrel monkey's handedness for unimanual and bimanual coordinated tasks. Anim. Behav. 83:635-643.
54. Meunier, H., C. Blois-Heulin, and J. Vauclair 2011. A new tool for measuring hand preference in non-human primates: adaptation of Bishop's Quantifying Hand Preference task for Olive baboons. Behav. Brain Res. 218:1-7.
55. Murata, Y., N. Higo, T. Oishi, A. Yamashita, K. Matsuda, M. Hayashi, et al. 2008. Effects of motor training on the recovery of manual dexterity after primary motor cortex lesion in macaque monkeys. J. Neurophysiol. 99:773-786.
56. Nudo, R. J., W. M. Jenkins, M. M. Merzenich, T. Prejean, and R. Grenda 1992. Neurophysiological correlates of hand preference in primary motor cortex of adult squirrel monkeys. J. Neurosci. 12:2918-2947.
57. Oldfield, R. C. 1971. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97-113.
58. Papademetriou, E., C. F. Sheu, and G. F. Michel 2005. A meta-analysis of primate hand preferences, particularly for reaching. J. Comp. Psychol. 119:33-48.
59. Porter, R., and R. Lemon 1993. Corticospinal function and voluntary movement. Clarendon Press, Oxford.
60. Pouydebat, E., E. Reghem, P. Gorce, and V. Bels 2010. Influence of the task on hand preference: individual differences among gorillas (Gorilla gorilla gorilla). Folia Primatol. (Basel) 81:273-281.
61. Raymond, M., and D. Pontier 2004. Is there geographical variation in human handedness? Laterality 9:35-51.
62. Raymond, M., D. Pontier, A. B. Dufour, and A. P. Moller 1996. Frequency-dependent maintenance of left handedness in humans. Proc. Biol. Sci. 263:1627-1633.
63. Rogers, L. J. 2009. Hand and paw preferences in relation to the lateralized brain. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364:943-954.
64. Rohr, L. E. 2006. Gender-specific movement strategies using a computer-pointing task. J. Mot. Behav. 38:431-437.
65. Rouiller, E. M., X. H. Yu, V. Moret, A. Tempini, M. Wiesendanger, and F. Liang 1998. Dexterity in adult monkeys following early lesion of the motor cortical hand area: the role of cortex adjacent to the lesion. Eur. J. Neurosci. 10:729-740.
66. Schaafsma, S. M., B. J. Riedstra, K. A. Pfannkuche, A. Bouma, and T. G. Groothuis 2009. Epigenesis of behavioural lateralization in humans and other animals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364:915-927.
67. Schmidlin, E., M. Kaeser, A. D. Gindrat, J. Savidan, P. Chatagny, S. Badoud, et al. 2011. Behavioral assessment of manual dexterity in non-human primates. J. Vis. Exp. 57:3258.
68. Schmitt, V., S. Melchisedech, K. Hammerschmidt, and J. Fischer 2008. Hand preferences in Barbary macaques (Macaca sylvanus). Laterality 13:143-157.
69. Serrien, D. J., R. B. Ivry, and S. P. Swinnen 2006. Dynamics of hemispheric specialization and integration in the context of motor control. Nat. Rev. Neurosci. 7:160-166.
70. Sherwood, C. C., E. Wahl, J. M. Erwin, P. R. Hof, and W. D. Hopkins 2007. Histological asymmetries of primary motor cortex predict handedness in chimpanzees (Pan troglodytes). J. Comp. Neurol. 503:525-537.
71. Singer, S. S., and M. H. Schwibbe 1999. Right or left, hand or mouth: general-specific preferences in marmosets and tamarins. Behaviour 136:119-145.
72. Spinozzi, G., M. G. Castorina, and V. Truppa 1998. Hand preferences in unimanual and coordinated-bimanual tasks by tufted capuchin monkeys (Cebus apella). J. Comp. Psychol. 112:183-191.
73. Spinozzi, G., T. Lagana, and V. Truppa 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.
74. Triggs, W. J., R. Calvanio, M. Levine, R. K. Heaton, and K. M. Heilman 2000. Predicting hand preference with performance on motor tasks. Cortex 36:679-689.
75. Uomini, N. T. 2009. The prehistory of handedness: archaeological data and comparative ethology. J. Hum. Evol. 57:411-419.
76. Vauclair, J., A. Meguerditchian, and W. D. Hopkins 2005. Hand preferences for unimanual and coordinated bimanual tasks in baboons (Papio anubis). Brain Res. Cogn. Brain Res. 25:210-216.
77. Ward, J. P., G. W. Milliken, D. L. Dodson, D. K. Stafford, and M. Wallace 1990. Handedness as a function of sex and age in a large population of Lemur. J. Comp. Psychol. 104:167-173.
78. Ward, J. P., G. W. Milliken, and D. K. Stafford 1993. Patterns of lateralized behavior in prosimians. Pp. 43-74 in J. P. Ward and W. D. Hopkins, eds. Primate laterality: current behavioral evidence of primate asymmetries. Springer, New-York, NY.
79. Wesley, M. J., S. Fernandez-Carriba, A. Hostetter, D. Pilcher, S. Poss, and W. D. Hopkins 2001. Factor analysis of multiple measures of hand use in captive chimpanzees: an alternative approach to the assessment of handedness in non-human primates. Int. J. Primatol. 23:1155-1168.
80. Westergaard, G. C., and I. D. Lussier 1999. Left-handedness and longevity in primates. Int. J. Neurosci. 99:79-87.
81. Westergaard, G. C., and S. J. Suomi 1996. Hand preference for a bimanual task in tufted capuchins (Cebus apella) and rhesus macaques (Macaca mulatta). J. Comp. Psychol. 110:406-411.
82. Westergaard, G. C., M. Champoux, and S. J. Suomi 1997. Hand preference in infant rhesus macaques (Macaca mulatta). Child Dev. 68:387-393.
83. Westergaard, G. C., I. D. Lussier, and J. D. Higley 2001a. Familial influences on hand preference: genotypic variation between closely related primate species. Dev. Neuropsychol. 20:605-617.
84. Westergaard, G. C., I. D. Lussier, and J. D. Higley 2001b. Between-species variation in the development of hand preference among macaques. Neuropsychologia 39:1373-1378.
85. Zhao, D., W. D. Hopkins, and B. Li 2012. Handedness in nature: first evidence on manual laterality on bimanual coordinated tube task in wild primates. Am. J. Phys. Anthropol. 148:36-44.