Experimental Brain Research

, Volume 233, Issue 3, pp 829–837 | Cite as

Handedness influences intermanual transfer in chimpanzees (Pan troglodytes) but not rhesus monkeys (Macaca mulatta)

  • Emily R. Boeving
  • Agnès Lacreuse
  • William D. Hopkins
  • Kimberley A. Phillips
  • Melinda A. Novak
  • Eliza L. Nelson
Research Article


Intermanual transfer refers to an effect, whereby training one hand to perform a motor task improves performance in the opposite untrained hand. We tested the hypothesis that handedness facilitates intermanual transfer in two nonhuman primate species: rhesus monkeys (N = 13) and chimpanzees (N = 52). Subjects were grouped into one of four conditions: (1) left-handers trained with the left (dominant) hand; (2) left-handers trained with the right (nondominant) hand; (3) right-handers trained with the left (nondominant) hand; and (4) right-handers trained with the right (dominant) hand. Intermanual transfer was measured using a task where subjects removed a Life Savers® candy (monkeys) or a washer (chimpanzees) from metal shapes. Transfer was measured with latency by comparing the average time taken to solve the task in the first session with the trained hand compared to the first session with the untrained hand. Hypotheses and predictions were derived from three models of transfer: access: benefit training with nondominant hand; proficiency: benefit training with dominant hand; and cross-activation: benefit irrespective of trained hand. Intermanual transfer (i.e., shorter latency in untrained hand) occurred regardless of whether monkeys trained with the dominant hand or nondominant hand, supporting the cross-activation model. However, transfer was only observed in chimpanzees that trained with the dominant hand. When handedness groups were examined separately, the transfer effect was only significant for right-handed chimpanzees, partially supporting the proficiency model. Findings may be related to neurophysiological differences in motor control as well as differences in handedness patterning between rhesus monkeys and chimpanzees.


Handedness Hand preference Intermanual transfer Rhesus monkey Chimpanzee 


  1. Ammons R (1958) Le moevement. In: Seward GS, Seward JP (eds) Current psychological issues. Holt, New York, pp 146–183Google Scholar
  2. Annett M (2002) Handedness and brain asymmetry: the right shift theory. Psychology Press, HoveGoogle Scholar
  3. Bachevalier J, Hagger C (1991) Sex differences in the development abilities in primates. Psychoneuroendocrinology 16:177–188PubMedCrossRefGoogle Scholar
  4. Beck CHM, Barton RL (1972) Deviation and laterality of hand preference in monkeys. Cortex 8(S4):339–363PubMedCrossRefGoogle Scholar
  5. Bennett AJ, Suomi SJ, Hopkins WD (2008) Effects of early adverse experiences on behavioural lateralization in rhesus monkeys (Macaca mulatta). Laterality 13(3):282–292PubMedGoogle Scholar
  6. Brinkman J, Kuypers HGJM (1973) Cerebral control of contralateral and ipsilateral arm, hand and finer movements in the split-brain rhesus monkey. Brain 96:653–674PubMedCrossRefGoogle Scholar
  7. Deuel RK, Dunlop NL (1980) Hand preference in the rhesus monkeys: implications for the study of cerebral dominance. Arch Neurol 37(4):217–221PubMedCrossRefGoogle Scholar
  8. Gash DM, Zhang Z, Umberger G, Mahood K, Smith M, Smith C, Gerhardt GA (1999) An automated movement assessment panel for upper limb motor functions in rhesus monkeys and humans. J Neurosci Methods 89(2):111–117PubMedCrossRefGoogle Scholar
  9. Halsband U (1992) Left hemisphere preponderance in trajectorial learning. Neuroreport 3:397–400PubMedCrossRefGoogle Scholar
  10. Hammond G (2002) Correlates of human handedness in primary motor cortex: a review and hypothesis. Neurosci Biobehav Rev 26(S3):285–292PubMedCrossRefGoogle Scholar
  11. Hikosaka O, Rand MK, Nakamura K, Miyachi S, Kitahuchi K, Sakai K, Lu X, Shimo Y (2002) Long-term retention of motor skill in macaque monkeys and humans. Exp Brain Res 147:494–504PubMedCrossRefGoogle Scholar
  12. Hopkins WD (1995) Hand preferences for a coordinated bimanual task in 110 chimpanzees (Pan troglodytes): cross-sectional analysis. J Comp Psychol 105:178–190Google Scholar
  13. Hopkins WD (2006) Comparative and familial analysis of handedness in great apes. Psychol Bull 132(S4):538–559PubMedCentralPubMedCrossRefGoogle Scholar
  14. Hopkins WD, Washburn DA, Berke L, Williams M (1992) Behavioral asymmetries of psychomotor performance in rhesus monkeys (Macaca mulatta): a disassociation between hand preference and skill. J Comp Psychol 106(4):392–397PubMedCrossRefGoogle Scholar
  15. Hopkins WD, Cantalupo C, Wesley MJ, Hostetter A, Pilcher D (2002) Group morphology and hand use in chimpanzees (Pan troglodytes): evidence of a left hemisphere specialization in motor skill. J Exp Psychol Gen 131:412–423PubMedCentralPubMedCrossRefGoogle Scholar
  16. Hopkins WD, Wesley MJ, Izard MK, Schapiro M (2004) Chimpanzees (Pan troglodytes) are predominately right handed: replications in three populations of apes. Behav Neurosci 118(S3):659–663PubMedCentralPubMedCrossRefGoogle Scholar
  17. Hopkins WD, Phillips KA, Bania A, Calcutt SE, Gardner M, Russell JL, Schaeffer J, Lonsdorf EV, Ross SR, Schapiro SJ (2011) Hand preference for coordinated bimanual actions in 777 great apes: implications for the evolution of handedness in hominins. J Hum Evol 60(S5):605–611PubMedCentralPubMedCrossRefGoogle Scholar
  18. Kuypers HGJM (1982) A new look at the motor system. Prog Brain Res 57:381–403PubMedCrossRefGoogle Scholar
  19. Lacreuse A, Herndon JG (2003) Effects of estradiol and aging on fine motor performance in female rhesus monkeys. Horm Behav 43:359–366PubMedCrossRefGoogle Scholar
  20. Lacreuse A, Diehl MM, Goh MY, Hall MJ, Volk AM, Chhabra RK, Herndon JG (2005) Sex differences in age-related motor slowing in the rhesus monkey: behavioral and neuroimaging data. Neurobiol Aging 26:543–551PubMedCrossRefGoogle Scholar
  21. Laszlo J, Baguley RA, Bairstow PJ (1970) Bilateral transfer in tapping skill in the absence of peripheral information. J Motor Behav 2(S4):261–271CrossRefGoogle Scholar
  22. Lee M, Hinder M, Gandevia S, Carroll T (2010) The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice. J Physiol 588:201–212PubMedCentralPubMedCrossRefGoogle Scholar
  23. Llorente M, Riba D, Laia P, Marina M, Monsterrat C, Olga F (2011) Population-level right-handedness for a coordinated bimanual task in naturalistic housed chimpanzees: replication and extension in 114 from Zambia and Spain. Am J Primatol 73:281–290PubMedCrossRefGoogle Scholar
  24. MacNeilage PF (2007) Present status of the postural origins theory. In: Hopkins WD (ed) The evolution of hemispheric specialization in primates. Elsevier, Oxford, pp 59–91Google Scholar
  25. MacNeilage PF, Studdert-Kennedy MG, Lindblom B (1987) Primate handedness reconsidered. Behav Brain Sci 10:247–303CrossRefGoogle Scholar
  26. Marchant LF, McGrew WC (2013) Handedness is more than laterality: lessons from chimpanzees. Ann NY Acad Sci 1288:1–8PubMedCrossRefGoogle Scholar
  27. McGrew WC, Marchant LF (1997) On the other hand: current issues in and meta-analysis of the behavioral laterality of hand function in nonhuman primates. Yearb Phys Anthropol 40:201–232CrossRefGoogle Scholar
  28. Meguerditchian A, Vauclair J, Hopkins WD (2013) On the origins of human handedness and language: a comparative review of hand preference for bimanual coordinated actions and gestural communication in nonhuman primates. Dev Psychobiol 55(6):637–650PubMedCrossRefGoogle Scholar
  29. Mostafa AA, Salomoncyzk D, Cressman EK, Henriques DYP (2014) Intermanual transfer and proprioceptive recalibration following training with translated visual feedback of the hand. Exp Brain Res 232(6):1639–1651PubMedCrossRefGoogle Scholar
  30. Mutha PK, Haaland KY, Sainburg RL (2013) Rethinking motor lateralization: specialized but complementary mechanisms for motor control of each arm. PLoS One 8(3):1–10CrossRefGoogle Scholar
  31. Nakajima K, Maier MA, Kirkwood PA, Lemon RN (2000) Striking differences in transmission of corticospinal excitation to upper limb motoneurons in two primate species. J Neurophysiol 84:698–709PubMedGoogle Scholar
  32. Nelson EL, Emery MS, Babcock SM, Novak MFSX, Suomi SJ, Novak MA (2011) Head orientation and handedness trajectory in rhesus monkey infants (Macaca mulatta). Dev Psychobiol 53:246–255PubMedCentralPubMedCrossRefGoogle Scholar
  33. Obayashi S, Suhara T, Kawabe K, Okauchi T, Maeda J, Nagai Y, Iriki A (2003) Fronto-parieto-cerebellar interaction associated with intermanual transfer of monkey tool-use learning. Neurosci Lett 339:123–126PubMedCrossRefGoogle Scholar
  34. Papademetriou D, Sheu CF, Michel GF (2005) A meta-analysis of primate hand preference, particularly for reaching. J Comp Psychol 119(1):33–48PubMedCrossRefGoogle Scholar
  35. Parlow SE, Kinsbourne M (1989) Asymmetrical transfer of training between hands: implications for interhemispheric communication in normal brain. Brain Cogn 11:98–113PubMedCrossRefGoogle Scholar
  36. Phillips KA, Schaeffer JA, Hopkins WD (2013) Corpus callosal microstructure influences intermanual transfer in chimpanzees. Front Syst Neurosci 7(125):1–6Google Scholar
  37. Schulze K, Luders E, Lutz J (2002) Intermanual transfer in a simple motor task. Cortex 38(S5):805–815PubMedCrossRefGoogle Scholar
  38. Smith CD, Umberger GH, Manning EL, Slevin JT, Wekstein DR, Schmidt FA, Markesbery WR, Zhang Z, Gerhardt GA, Kryscio RJ, Gash DM (1999) Critical decline in fine motor hand movements in human aging. Neurology 53:1458–1461PubMedCrossRefGoogle Scholar
  39. Taylor HG, Heilman KM (1980) Left-hemisphere dominance in right handers. Cortex 16:587–603PubMedCrossRefGoogle Scholar
  40. Wesley MJ, Ferandez-Carriba S, Hostetter A, Pilcher D (2002) Factor analysis of multiple measures of hand use in captive chimpanzees: an alternative approach to the assessment of handedness in nonhuman primates. Int J Primatol 23:1155–1168CrossRefGoogle Scholar
  41. Westergaard GC, Champoux M, Suomi SJ (1997) Hand preference in infant rhesus macaque (Macaca mulatta). Child Dev 68(3):387–393PubMedGoogle Scholar
  42. Zhang Z, Andersen A, Smith C, Grondin R, Gerhardt G, Gash D (2000) Motor slowing and parkinsonian signs in aging rhesus monkeys mirror human aging. J Gerontol A Biol Sci Med Sci 55:B473–B480PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Emily R. Boeving
    • 1
  • Agnès Lacreuse
    • 2
  • William D. Hopkins
    • 3
    • 4
  • Kimberley A. Phillips
    • 5
    • 6
  • Melinda A. Novak
    • 2
  • Eliza L. Nelson
    • 1
  1. 1.Department of PsychologyFlorida International UniversityMiamiUSA
  2. 2.Department of Psychological and Brain SciencesUniversity of Massachusetts AmherstAmherstUSA
  3. 3.Neuroscience Institute and Language Research CenterGeorgia State UniversityAtlantaUSA
  4. 4.Division of Developmental and Cognitive NeuroscienceYerkes National Primate Research CenterAtlantaUSA
  5. 5.Department of PsychologyTrinity UniversitySan AntonioUSA
  6. 6.Southwest National Primate Research CenterTexas Biomedical Research InstituteSan AntonioUSA

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