Experimental Brain Research

, Volume 236, Issue 4, pp 1091–1103 | Cite as

Gaze anchoring guides real but not pantomime reach-to-grasp: support for the action–perception theory

  • Jessica R. Kuntz
  • Jenni M. Karl
  • Jon B. Doan
  • Ian Q. Whishaw
Research Article

Abstract

Reach-to-grasp movements feature the integration of a reach directed by the extrinsic (location) features of a target and a grasp directed by the intrinsic (size, shape) features of a target. The action-perception theory suggests that integration and scaling of a reach-to-grasp movement, including its trajectory and the concurrent digit shaping, are features that depend upon online action pathways of the dorsal visuomotor stream. Scaling is much less accurate for a pantomime reach-to-grasp movement, a pretend reach with the target object absent. Thus, the action-perception theory proposes that pantomime movement is mediated by perceptual pathways of the ventral visuomotor stream. A distinguishing visual feature of a real reach-to-grasp movement is gaze anchoring, in which a participant visually fixates the target throughout the reach and disengages, often by blinking or looking away/averting the head, at about the time that the target is grasped. The present study examined whether gaze anchoring is associated with pantomime reaching. The eye and hand movements of participants were recorded as they reached for a ball of one of three sizes, located on a pedestal at arms’ length, or pantomimed the same reach with the ball and pedestal absent. The kinematic measures for real reach-to-grasp movements were coupled to the location and size of the target, whereas the kinematic measures for pantomime reach-to-grasp, although grossly reflecting target features, were significantly altered. Gaze anchoring was also tightly coupled to the target for real reach-to-grasp movements, but there was no systematic focus for gaze, either in relation with the virtual target, the previous location of the target, or the participant’s reaching hand, for pantomime reach-to-grasp. The presence of gaze anchoring during real vs. its absence in pantomime reach-to-grasp supports the action–perception theory that real, but not pantomime, reaches are online visuomotor actions and is discussed in relation with the neural control of real and pantomime reach-to-grasp movements.

Keywords

Action–perception Pantomime reaching Reach-to-grasp Dorsal stream Ventral stream Visually guided reaching Visual attention 

Notes

Acknowledgements

This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) [JRK], NSERC Discovery Grant [JBD], and NSERC Discovery Grant [JMK]. The authors would like to thank Tsz Yin (Ian) Fung for his help with data collection.

Compliance with ethical standards

Conflict of interest

The authors declare no competing financial interests.

References

  1. Arbib MA (1981). Perceptual structures and distributed motor control. Comprehensive physiologyGoogle Scholar
  2. Bingham G, Coats R, Mon-Williams M (2007) Natural prehension in trials without haptic feedback but only when calibration is allowed. Neuropsychologia 45(2):288–294.  https://doi.org/10.1016/j.neuropsychologia.2006.07.011 CrossRefPubMedGoogle Scholar
  3. Bridge H, Thomas OM, Minini L, Cavina-Pratesi C, Milner AD, Parker AJ (2013) Structural and Functional changes across the visual cortex of a patient with visual form agnosia. J Neurosci 33(31):12779–12791.  https://doi.org/10.1523/Jneurosci.4853-12.2013 CrossRefPubMedGoogle Scholar
  4. Casarotti M, Lisi M, Umilta C, Zorzi M (2012) Paying attention through eye movements: a computational investigation of the premotor theory of spatial attention. J Cogn Neurosci 24(7):1519–1531.  https://doi.org/10.1162/jocn_a_00231 CrossRefPubMedGoogle Scholar
  5. Cavina-Pratesi C, Monaco S, Fattori P, Galletti C, McAdam TD, Quinlan DJ, Goodale MA, Culham JC (2010) Functional magnetic resonance imaging reveals the neural substrates of arm transport and grip formation in reach-to-grasp actions in humans. J Neurosci 30(31):10306–10323.  https://doi.org/10.1523/Jneurosci.2023-10.2010 CrossRefPubMedGoogle Scholar
  6. Cavina-Pratesi C, Kuhn G, Ietswaart M, Milner AD (2011). The magic grasp: motor expertise in deception. Plos One, 6(2), e16568Google Scholar
  7. Chan J, Heath M (2017) Haptic feedback attenuates illusory bias in pantomime-grasping: evidence for a visuo-haptic calibration. Exp Brain Res 235(4):1041–1051.  https://doi.org/10.1007/s00221-016-4860-9 CrossRefPubMedGoogle Scholar
  8. Coats R, Bingham GP, Mon-Williams M (2008) Calibrating grasp size and reach distance: interactions reveal integral organization of reaching-to-grasp movements. Exp Brain Res 189(2):211–220.  https://doi.org/10.1007/s00221-008-1418-5 CrossRefPubMedGoogle Scholar
  9. Cohen NR, Cross ES, Tunik E, Grafton ST, Culham JC (2009) Ventral and dorsal stream contributions to the online control of immediate and delayed grasping: a TMS approach. Neuropsychologia 47(6):1553–1562.  https://doi.org/10.1016/j.neuropsychologia.2008.12.034 CrossRefPubMedGoogle Scholar
  10. Culham JC, Valyear KF (2006) Human parietal cortex in action. Curr Opin Neurobiol 16(2):205–212.  https://doi.org/10.1016/j.conb.2006.03.005 CrossRefPubMedGoogle Scholar
  11. de Bruin N, Sacrey L-AR, Brown LA, Doan J, Whishaw IQ (2008) Visual guidance for hand advance but not hand withdrawal in a reach-to-eat task in adult humans: reaching is a composite movement. J Motor Behav 40(4):337–346CrossRefGoogle Scholar
  12. De Stefani E, Innocenti A, De Marco D, Busiello M, Ferri F, Costantini M, Gentilucci M (2014) The spatial alignment effect in near and far space: a kinematic study. Exp Brain Res 232(7):2431–2438.  https://doi.org/10.1007/s00221-014-3943-8 CrossRefPubMedGoogle Scholar
  13. Fukui T, Inui T (2013) Utilization of visual feedback of the hand according to target view availability in the online control of prehension movements. Hum Mov Sci 32(4):580–595.  https://doi.org/10.1016/j.humov.2013.03.004 CrossRefPubMedGoogle Scholar
  14. Gentilucci M, Chieffi S, Daprati E, Saetti MC, Toni I (1996) Visual illusion and action. Neuropsychologia 34(5):369–376CrossRefPubMedGoogle Scholar
  15. Goldenberg G (2017) Facets of pantomime. J Int Neuropsychol Soc 23(2):121–127.  https://doi.org/10.1017/S1355617716000989 CrossRefPubMedGoogle Scholar
  16. Goodale MA, Milner AD, Jakobson LS, Carey DP (1991) A neurological dissociation between perceiving objects and grasping them. Nature 349(6305):154–156. doi: https://doi.org/10.1038/349154a0 CrossRefPubMedGoogle Scholar
  17. Goodale MA, Jakobson LS, Keillor JM (1994) Differences in the visual control of pantomimed and natural grasping movements. Neuropsychologia 32(10):1159–1178.  https://doi.org/10.1016/0028-3932(94)90100-7 CrossRefPubMedGoogle Scholar
  18. Hall LA, Karl JM, Thomas BL, Whishaw IQ (2014) Reach and Grasp reconfigurations reveal that proprioception assists reaching and hapsis assists grasping in peripheral vision. Exp Brain Res 232(9):2807–2819.  https://doi.org/10.1007/s00221-014-3945-6 CrossRefPubMedGoogle Scholar
  19. Hoeren M, Kummerer D, Bormann T, Beume L, Ludwig VM, Vry MS, Mader I, Rijntjes M, Kaller CP, Weiller C (2014) Neural bases of imitation and pantomime in acute stroke patients: distinct streams for praxis. Brain 137:2796–2810.  https://doi.org/10.1093/brain/awu203 CrossRefPubMedGoogle Scholar
  20. Holmes SA, Lohmus J, McKinnon S, Mulla A, Heath M (2013) Distinct visual cues mediate aperture shaping for grasping and pantomime-grasping tasks. J Motor Behav 45(5):431–439.  https://doi.org/10.1080/00222895.2013.818930 CrossRefGoogle Scholar
  21. James TW, Culham J, Humphrey GK, Milner AD, Goodale MA (2003) Ventral occipital lesions impair object recognition but not object-directed grasping: an fMRI study. Brain 126:2463–2475.  https://doi.org/10.1093/brain/awg248 CrossRefPubMedGoogle Scholar
  22. Jazi SD, Heath M (2017) The spatial relations between stimulus and response determine an absolute visuo-haptic calibration in pantomime-grasping. Brain Cogn 114:29–39.  https://doi.org/10.1016/j.bandc.2017.03.002 CrossRefGoogle Scholar
  23. Jeannerod M (1981). Intersegmental coordination during reaching at natural visual objects. Attention and Performance IXGoogle Scholar
  24. Jeannerod M, Decety J, Michel F (1994) Impairment of grasping movements following a bilateral posterior parietal lesion. Neuropsychologia 32(4):369–380.  https://doi.org/10.1016/0028-3932(94)90084-1 CrossRefPubMedGoogle Scholar
  25. Karl JM, Sacrey L-AR, Doan JB, Whishaw IQ (2012) Hand shaping using hapsis resembles visually guided hand shaping. Exp Brain Res 219(1):59–74CrossRefPubMedGoogle Scholar
  26. Karl JM, Schneider LR, Whishaw IQ (2013) Nonvisual learning of intrinsic object properties in a reaching task dissociates grasp from reach. Exp Brain Res 225(4):465–477CrossRefPubMedGoogle Scholar
  27. Króliczak G, Cavina-Pratesi C, Goodman DA, Culham JC (2007) What does the brain do when you fake it? An fMRI study of pantomimed and real grasping. J Neurophysiol 97(3):2410–2422.  https://doi.org/10.1152/jn.00778.2006 CrossRefPubMedGoogle Scholar
  28. Kuntz JR, Whishaw IQ (2016) Synchrony of the reach and the grasp in pantomime reach-to-grasp. Exp Brain Res 234(11):3291–3303.  https://doi.org/10.1007/s00221-016-4727-0 CrossRefPubMedGoogle Scholar
  29. Milner AD, Goodale MA (2006). The visual brain in action. Oxford University PressGoogle Scholar
  30. Milner AD, Goodale MA (2008) Two visual systems re-viewed. Neuropsychologia 46(3):774–785.  https://doi.org/10.1016/j.neuropsychologia.2007.10.005 CrossRefPubMedGoogle Scholar
  31. Milner A, Dijkerman H, Pisella L, McIntosh R, Tilikete C, Vighetto A, Rossetti Y (2001) Grasping the past: delay can improve visuomotor performance. Curr Biol 11(23):1896–1901CrossRefPubMedGoogle Scholar
  32. Neggers SFW, Bekkering H (2000) Ocular gaze is anchored to the target of an ongoing pointing movement. J Neurophysiol 83(2):639–651CrossRefPubMedGoogle Scholar
  33. Posner MI (1980) Orienting of attention. Q J Exp Psychol 32(1):3–25CrossRefPubMedGoogle Scholar
  34. Prablanc C, Echallier JE, Jeannerod M, Komilis E (1979) Optimal response of eye and hand motor systems in pointing at a visual target. 2. Static and dynamic visual cues in the control of hand movement. Biol Cybern 35(3):183–187.  https://doi.org/10.1007/Bf00337063 CrossRefPubMedGoogle Scholar
  35. Rinsma T, van der Kamp J, Dicks M, Canal-Bruland R (2017) Nothing magical: pantomimed grasping is controlled by the ventral system. Exp Brain Res 235(6):1823–1833.  https://doi.org/10.1007/s00221-016-4868-1 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Sacrey L-AR, Whishaw IQ (2012a) Subsystems of sensory attention for skilled reaching: Vision for transport and pre-shaping and somatosensation for grasping, withdrawal and release. Behav Brain Res 231(2):356–365.  https://doi.org/10.1016/j.bbr.2011.07.031 CrossRefPubMedGoogle Scholar
  37. Sacrey LAR, Whishaw IQ (2012b) Subsystems of sensory attention for skilled reaching: Vision for transport and pre-shaping and somatosensation for grasping, withdrawal and release. Behav Brain Res 231(2):356–365.  https://doi.org/10.1016/j.bbr.2011.07.031 CrossRefPubMedGoogle Scholar
  38. Vry MS, Tritschler LC, Hamzei F, Rijntjes M, Kaller CP, Hoeren M, Umarova R, Glauche V, Hermsdoerfer J, Goldenberg G, Hennig J, Weiller C (2015) The ventral fiber pathway for pantomime of object use. Neuroimage 106:252–263.  https://doi.org/10.1016/j.neuroimage.2014.11.002 CrossRefPubMedGoogle Scholar
  39. Westwood DA, Chapman CD, Roy EA (2000). Pantomimed actions may be controlled by the ventral visual stream. Exp Brain Res, 130(4)Google Scholar
  40. Whishaw IQ, Suchowersky O, Davis L, Sarna J, Metz GA, Pellis SM (2002) Impairment of pronation, supination, and body co-ordination in reach-to-grasp tasks in human Parkinson’s disease (PD) reveals homology to deficits in animal models. Behav Brain Res 133(2):165–176CrossRefPubMedGoogle Scholar
  41. Whishaw IQ, Karl JM, Humphrey NK (2016) Dissociation of the reach and the grasp in the destriate (V1) monkey Helen: a new anatomy for the dual visuomotor channel theory of reaching. Exp Brain Res 234(8):2351–2362.  https://doi.org/10.1007/s00221-016-4640-6 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Neuroscience, Canadian Centre for Behavioral NeuroscienceUniversity of LethbridgeLethbridgeCanada
  2. 2.Department of PsychologyThompson Rivers UniversityKamloopsCanada
  3. 3.Engineering and Human Performance Lab, Department of Kinesiology and Physical EducationUniversity of LethbridgeLethbridgeCanada

Personalised recommendations