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.
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References
Berman RA, Wurtz RH (2010) Functional identification of a pulvinar path from superior colliculus to cortical area MT. J Neurosci 30:6342–6354
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
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
Brozzoli C, Pavani F, Urquizar C, Cardinali L, Farnè A (2009) Grasping actions remap peripersonal space. NeuroReport 20:913–917
Brozzoli C, Cardinali L, Pavani F, Farnè A (2010) Action specific remapping of peripersonal space. Neuropsychologia 48:796–802
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)
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
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
Cisek P, Kalaska JF (2010) Neural mechanisms for interacting with a world full of action choices. Annu Rev Neurosci 33:269–298
Cohen YE, Andersen RA (2002) A common reference frame for movement plans in the posterior parietal cortex. Nature Rev Neurosci 3:553–562
Cooke DF, Graziano MS (2003) Defensive movements evoked by air puff in monkeys. J Neurophysiol 90:3317–3329
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
Coxon JP, Stinear CM, Byblow WD (2007) Selective inhibition of movement. J Neurophysiol 97:2480–2489
Crawford JD, Medendorp WP, Marotta JJ (2004) Spatial transformations for eye-hand coordination. J Neurophysiol 92:10–19
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
Duhamel JR, Colby CL, Goldberg ME (1998) Ventral intraparietal area of the macaque: congruent visual and somatic response properties. J Neurophysiol 79:126–136
Evarts EV (1974) Precentral and postcentral cortical activity in association with visually triggered movement. J Neurophysiol 37:373–381
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
Farnè A, Demattè ML, Ladavas E (2005) Neuropsychological evidence of modular organization of the near peripersonal space. Neurology 13:1754–1758
Fogassi L, Luppino G (2005) Motor functions of the parietal lobe. Curr Opin Neurobiol 15:626–631
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
Glennerster A, Hansard ME, Fitzgibbon AW (2001) Fixation could simplify, not complicate, the interpretation of retinal flow. Vision Res 41:815–834
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
Graziano MS, Gross CG (1998) Spatial maps for the control of movement. Curr Opin Neurobiol 8:195–201
Graziano MSA, Yap GS, Gross CG (1994) Coding of visual space by premotor neurons. Science 266:1054–1057
Graziano MSA, Hu XT, Gross CG (1997) Visuospatial properties of ventral premotor cortex. J Neurophysiol 77:2268–2292
Graziano MSA, Taylor CSR, Moore T (2002) Complex movements evoked by microstimulation of precentral cortex. Neuron 34:841–851
Kaas JH, Lyon DC (2007) Pulvinar contributions to the dorsal and ventral streams of visual processing in primates. Brain Res Rev 55:285–296
Kakei S, Hoffman DS, Strick PL (2001) Direction of action is represented in the ventral premotor cortex. Nat Neurosci 10:1020–1025
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
Làdavas E (2002) Functional and dynamic properties of visual peripersonal space. Trends Cogn Sci 6:17–22
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
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
Makin TR, Holmes NP, Ehrsson HH (2008) On the other hand: dummy hands and peripersonal space. Behav Brain Res 191:1–10
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
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
Maunsell JH, Newsome WT (1978) Visual processing in monkey extrastriate cortex. Annu Rev Neurosci 10:363–364
McGuire LMM, Sabes PN (2009) Sensory transformations and the use of multiple reference frames for reach planning. Nature Neurosci 12:1056–1061
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
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
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
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
Perry VH, Cowey A (1984) Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neurosci 12:1125–1137
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
Pesaran B, Nelson MJ, Andersen RA (2010) A relative position code for saccades in dorsal premotor cortex. J Neurosci 30:6527–6537
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
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
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
Rizzolatti G (1987) Functional organization of inferior area 6. Ciba Found Symp 132:171–186
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
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
Schlicht EJ, Schrater PR (2007) Impact of coordinate transformation uncertainty on human sensorimotor control. J Neurophysiol 97:4203–4214
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
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
Sincich LC, Park KF, Wohlgemuth MJ, Horton JC (2004) Bypassing V1: a direct geniculate input to area MT. Nat Neurosci 7:1123–1128
Snyder LH (2000) Coordinate transformations for eye and arm movements in the brain. Curr Opin Neurobiol 10:747–754
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
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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
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DOI: https://doi.org/10.1007/s00221-012-3089-5