Skip to main content
Log in

Keeping the world at hand: rapid visuomotor processing for hand–object interactions

  • Mini-Review
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

An Erratum to this article was published on 22 May 2012

Abstract

The existence of hand-centred visual processing has long been established in the macaque premotor cortex. These hand-centred mechanisms have been thought to play some general role in the sensory guidance of movements towards objects, or, more recently, in the sensory guidance of object avoidance movements. We suggest that these hand-centred mechanisms play a specific and prominent role in the rapid selection and control of manual actions following sudden changes in the properties of the objects relevant for hand–object interactions. We discuss recent anatomical and physiological evidence from human and non-human primates, which indicates the existence of rapid processing of visual information for hand–object interactions. This new evidence demonstrates how several stages of the hierarchical visual processing system may be bypassed, feeding the motor system with hand-related visual inputs within just 70 ms following a sudden event. This time window is early enough, and this processing rapid enough, to allow the generation and control of rapid hand-centred avoidance and acquisitive actions, for aversive and desired objects, respectively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Berman RA, Wurtz RH (2010) Functional identification of a pulvinar path from superior colliculus to cortical area MT. J Neurosci 30:6342–6354

    Article  PubMed  CAS  Google Scholar 

  • Bhattacharyya R, Musallam S, Andersen RA (2009) Parietal reach region encodes reach depth using retinal disparity and vergence angle signals. J Neurophysiol 102:805–816

    Article  PubMed  Google Scholar 

  • Boulinguez P, Jaffard M, Granjon L, Benraiss A (2008) Warning signals induce automatic EMG activations and proactive volitional inhibition: evidence from analysis of error distribution in simple RT. J Neurophysiol 99:1572–1578

    Article  PubMed  Google Scholar 

  • Brozzoli C, Pavani F, Urquizar C, Cardinali L, Farnè A (2009) Grasping actions remap peripersonal space. NeuroReport 20:913–917

    Article  PubMed  Google Scholar 

  • Brozzoli C, Cardinali L, Pavani F, Farnè A (2010) Action specific remapping of peripersonal space. Neuropsychologia 48:796–802

    Article  PubMed  CAS  Google Scholar 

  • Brozzoli C, Makin T, Cardinali L, Holmes NP, Farnè A (2011) Peripersonal space: a multisensory interface for body-object interactions. In: Murray MM, Wallace MT (eds) Frontiers in the neural bases of multisensory processes. CIBM, Lausanne (Switzerland)

    Google Scholar 

  • Buch ER, Mars RB, Boorman ED, Rushworth MFS (2010) A network centered on ventral premotor cortex exerts both facilitatory and inhibitory control over primary motor cortex during action reprogramming. J Neurosci 30:1395–1401

    Article  PubMed  CAS  Google Scholar 

  • Buneo CA, Andersen RA (2006) The posterior parietal cortex: sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia 44:2594–2606

    Article  PubMed  Google Scholar 

  • Cisek P, Kalaska JF (2010) Neural mechanisms for interacting with a world full of action choices. Annu Rev Neurosci 33:269–298

    Article  PubMed  CAS  Google Scholar 

  • Cohen YE, Andersen RA (2002) A common reference frame for movement plans in the posterior parietal cortex. Nature Rev Neurosci 3:553–562

    Article  CAS  Google Scholar 

  • Cooke DF, Graziano MS (2003) Defensive movements evoked by air puff in monkeys. J Neurophysiol 90:3317–3329

    Article  PubMed  Google Scholar 

  • Cooke DF, Taylor CSR, Moore T, Graziano MSA (2003) Complex movements evoked by microstimulation of the ventral intraparietal area. Proc Natl Acad Sci USA 100:6163–6168

    Article  PubMed  CAS  Google Scholar 

  • Coxon JP, Stinear CM, Byblow WD (2007) Selective inhibition of movement. J Neurophysiol 97:2480–2489

    Article  PubMed  Google Scholar 

  • Crawford JD, Medendorp WP, Marotta JJ (2004) Spatial transformations for eye-hand coordination. J Neurophysiol 92:10–19

    Article  PubMed  CAS  Google Scholar 

  • Davare M, Andres M, Cosnard G, Thonnard JL, Olivier E (2006) Dissociating the role of ventral and dorsal premotor cortex in precision grasping. J Neurosci 26:2260–2268

    Article  PubMed  Google Scholar 

  • Duhamel JR, Colby CL, Goldberg ME (1998) Ventral intraparietal area of the macaque: congruent visual and somatic response properties. J Neurophysiol 79:126–136

    PubMed  CAS  Google Scholar 

  • Evarts EV (1974) Precentral and postcentral cortical activity in association with visually triggered movement. J Neurophysiol 37:373–381

    PubMed  CAS  Google Scholar 

  • Farnè A, Roy AC, Paulignan Y, Rode G, Rossetti Y, Boisson D, Jeannerod M (2003) Visuo-motor control of the ipsilateral hand: evidence from right brain-damaged patients. Neuropsychologia 41:739–757

    Article  PubMed  Google Scholar 

  • Farnè A, Demattè ML, Ladavas E (2005) Neuropsychological evidence of modular organization of the near peripersonal space. Neurology 13:1754–1758

    Article  Google Scholar 

  • Fogassi L, Luppino G (2005) Motor functions of the parietal lobe. Curr Opin Neurobiol 15:626–631

    Article  PubMed  CAS  Google Scholar 

  • Gardner JL, Merriam EP, Movshon JA, Heeger DJ (2008) Maps of visual space in human occipital cortex are retinotopic, not spatiotopic. J Neurosci 28:3988–3999

    Article  PubMed  CAS  Google Scholar 

  • Glennerster A, Hansard ME, Fitzgibbon AW (2001) Fixation could simplify, not complicate, the interpretation of retinal flow. Vision Res 41:815–834

    Article  PubMed  CAS  Google Scholar 

  • Graziano MSA (1999) Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position. Proc Natl Acad Sci USA 96:10418–10421

    Article  PubMed  CAS  Google Scholar 

  • Graziano MS, Gross CG (1998) Spatial maps for the control of movement. Curr Opin Neurobiol 8:195–201

    Article  PubMed  CAS  Google Scholar 

  • Graziano MSA, Yap GS, Gross CG (1994) Coding of visual space by premotor neurons. Science 266:1054–1057

    Article  PubMed  CAS  Google Scholar 

  • Graziano MSA, Hu XT, Gross CG (1997) Visuospatial properties of ventral premotor cortex. J Neurophysiol 77:2268–2292

    PubMed  CAS  Google Scholar 

  • Graziano MSA, Taylor CSR, Moore T (2002) Complex movements evoked by microstimulation of precentral cortex. Neuron 34:841–851

    Article  PubMed  CAS  Google Scholar 

  • Kaas JH, Lyon DC (2007) Pulvinar contributions to the dorsal and ventral streams of visual processing in primates. Brain Res Rev 55:285–296

    Article  PubMed  Google Scholar 

  • Kakei S, Hoffman DS, Strick PL (2001) Direction of action is represented in the ventral premotor cortex. Nat Neurosci 10:1020–1025

    Article  Google Scholar 

  • Koch G, Franca M, Del Olmo MF, Cheeran BJ, Milton R, Alvarez Sauco M, Rothwell JC (2006) Time course of functional connectivity between dorsal premotor and contralateral motor cortex during movement selection. J Neurosci 26:7452–7459

    Article  PubMed  CAS  Google Scholar 

  • Làdavas E (2002) Functional and dynamic properties of visual peripersonal space. Trends Cogn Sci 6:17–22

    Article  Google Scholar 

  • Lewis JW, Van Essen DC (2000) Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J Comput Neurosci 428:112–137

    CAS  Google Scholar 

  • Lyon DC, Nassi JJ, Callaway EM (2010) A disynaptic relay from superior colliculus to dorsal stream visual cortex in macaque monkey. Neuron 65:270–279

    Article  PubMed  CAS  Google Scholar 

  • Makin TR, Holmes NP, Ehrsson HH (2008) On the other hand: dummy hands and peripersonal space. Behav Brain Res 191:1–10

    Article  PubMed  Google Scholar 

  • Makin TR, Holmes NP, Brozzoli C, Rossetti YRC, Farnè A (2009) Coding of visual space during motor preparation: approaching objects rapidly modulate corticospinal excitability in hand-centred coordinates. J Neurosci 29:11841–11851

    Article  PubMed  CAS  Google Scholar 

  • Marzocchi N, Breveglieri R, Galletti C, Fattori P (2008) Reaching activity in parietal area V6A of macaque: eye influence on arm activity or retinocentric coding of reaching movements? Eur J Neurosci 27:775–789

    Article  PubMed  Google Scholar 

  • Maunsell JH, Newsome WT (1978) Visual processing in monkey extrastriate cortex. Annu Rev Neurosci 10:363–364

    Article  Google Scholar 

  • McGuire LMM, Sabes PN (2009) Sensory transformations and the use of multiple reference frames for reach planning. Nature Neurosci 12:1056–1061

    Article  PubMed  CAS  Google Scholar 

  • Mushiake H, Tanatsugu Y, Tanji J (1997) Neuronal activity in the ventral part of premotor cortex during target-reach movement is modulated by direction of gaze. J Neurophysiol 78:567–571

    PubMed  CAS  Google Scholar 

  • O’Shea J, Sebastian C, Boorman ED, Johansen-Berg H, Rushworth MFS (2007) Functional specificity of human premotor-motor cortical interactions during action selection. Eur J Neurosci 26:2085–2095

    Article  PubMed  Google Scholar 

  • Paulignan Y, MacKenzie C, Marteniuk R, Jeannerod M (1991a) Selective perturbation of visual input during prehension movements. 1. The effects of changing object position. Exp Brain Res 83:502–512

    Article  PubMed  CAS  Google Scholar 

  • Paulignan Y, Jeannerod M, MacKenzie C, Marteniuk R (1991b) Selective perturbation of visual input during prehension movements. 2. The effects of changing object size. Exp Brain Res 87:407–420

    Article  PubMed  CAS  Google Scholar 

  • Perry VH, Cowey A (1984) Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neurosci 12:1125–1137

    Article  CAS  Google Scholar 

  • Pesaran B, Nelson MJ, Andersen RA (2006) Dorsal premotor neurons encode the relative position of the hand, eye, and goal during reach planning. Neuron 51:125–134

    Article  PubMed  CAS  Google Scholar 

  • Pesaran B, Nelson MJ, Andersen RA (2010) A relative position code for saccades in dorsal premotor cortex. J Neurosci 30:6527–6537

    Article  PubMed  CAS  Google Scholar 

  • Pettersson LG, Lundberg A, Alstermark B, Isa T, Tantisira B (1997) Effect of spinal cord lesions on forelimb target-reaching and on visually guided switching of target-reaching in the cat. Neurosci Res 29:241–256

    Article  PubMed  CAS  Google Scholar 

  • Pruszynski JA, Kurtzer I, Scott SH (2008) Rapid motor responses are appropriately tuned to the metrics of a visuo-spatial task. J Neurophysiol 100:224–238

    Article  PubMed  Google Scholar 

  • Reyes-Puerta V, Philipp R, Lindner W, Hoffmann KP (2010) Role of the rostral superior colliculus in gaze anchoring during reach movements. J Neurophysiol 103:3153–3166

    Article  PubMed  Google Scholar 

  • Rizzolatti G (1987) Functional organization of inferior area 6. Ciba Found Symp 132:171–186

    PubMed  CAS  Google Scholar 

  • Rizzolatti G, Scandolara C, Matelli M, Gentilucci M (1981) Afferent properties of periarcuate neurons in macque monkeys. II. Visual responses. Behav Brain Res 2:147–163

    Article  PubMed  CAS  Google Scholar 

  • Schicke T, Bauer F, Röder B (2009) Interactions of different body parts in peripersonal space: how vision of the foot influences tactile perception at the hand. Exp Brain Res 192:703–715

    Article  PubMed  Google Scholar 

  • Schlicht EJ, Schrater PR (2007) Impact of coordinate transformation uncertainty on human sensorimotor control. J Neurophysiol 97:4203–4214

    Article  PubMed  Google Scholar 

  • Schmolesky MT, Wang Y, Hanes DP, Thompson KG, Leutgeb S, Schall JD, Leventhal AG (1998) Signal timing across the macaque visual system. J Neurophysiol 79:3272–3278

    PubMed  CAS  Google Scholar 

  • Serino A, Canzoneri E, Avenanti A (2011) Fronto-parietal areas necessary for a multisensory representation of peripersonal space in humans: an rTMS study. J Cogn Neurosci 23:2956–2967

    Article  PubMed  Google Scholar 

  • Sincich LC, Park KF, Wohlgemuth MJ, Horton JC (2004) Bypassing V1: a direct geniculate input to area MT. Nat Neurosci 7:1123–1128

    Article  PubMed  CAS  Google Scholar 

  • Snyder LH (2000) Coordinate transformations for eye and arm movements in the brain. Curr Opin Neurobiol 10:747–754

    Article  PubMed  CAS  Google Scholar 

  • Stuphorn V, Bauswein E, Hoffmann KP (2000) Neurons in the primate superior colliculus coding for arm movements in gaze-related coordinates. J Neurophysiol 83:1283–1299

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tamar R. Makin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Makin, T.R., Holmes, N.P., Brozzoli, C. et al. Keeping the world at hand: rapid visuomotor processing for hand–object interactions. Exp Brain Res 219, 421–428 (2012). https://doi.org/10.1007/s00221-012-3089-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-012-3089-5

Keywords

Navigation