Abstract
The dual visuomotor channel theory proposes that prehension consists of a Reach that transports the hand in relation to an object’s extrinsic properties (e.g., location) and a Grasp that shapes the hand to an object’s intrinsic properties (e.g., size and shape). In central vision, the Reach and the Grasp are integrated but when an object cannot be seen, the movements can decompose with the Reach first used to locate the object and the Grasp postponed until it is assisted by touch. Reaching for an object in a peripheral visual field is an everyday act, and although it is reported that there are changes in Grasp aperture with target eccentricity, it is not known whether the configuration of the Reach and the Grasp also changes. The present study examined this question by asking participants to reach for food items at 0° or 22.5° and 45° from central gaze. Participants made 15 reaches for a larger round donut ball and a smaller blueberry, and hand movements were analyzed using frame-by-frame video inspection and linear kinematics. Perception of targets was degraded as participants could not identify objects in peripheral vision but did recognize their differential size. The Reach to peripheral targets featured a more dorsal trajectory, a more open hand, and less accurate digit placement. The Grasp featured hand adjustments or target manipulations after contact, which were associated with a prolonged Grasp duration. Thus, Grasps to peripheral vision did not consist only of a simple modification of visually guided reaching but included the addition of somatosensory assistance. The kinematic and behavioral changes argue that proprioception assists the Reach and touch assists the Grasp in peripheral vision, supporting the idea that Reach and Grasp movements are used flexibly in relation to sensory guidance depending upon the salience of target properties.
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References
Andersen RA, Andersen KN, Hwang EJ, Hauschild M (2014) Optic ataxia: from Balint’s syndrome to the parietal reach region. Neuron 81:967–983. doi:10.1016/j.neuron.2014.02.025
Ansuini C, Giosa L, Turella L, Altoe G, Castiello U (2008) An object for an action, the same object for other actions: effects on hand shaping. Exp Brain Res 185:111–119. doi:10.1007/s00221-007-1136-4
Bedell HE, Johnson CA (1984) The perceived size of targets in the peripheral and central visual fields. Ophthalmic Physiol Opt 4:123–131. doi:10.1111/j.1475-1313.1984.tb00345.x
Bernier PM, Grafton ST (2010) Human posterior parietal cortex flexibly determines reference frames for reaching based on sensory context. Neuron 68:776–788. doi:10.1016/j.neuron.2010.11.002
Binkofski F, Buccino G, Posse S, Seitz RJ, Rizzolatti G, Freund H (1999) A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. Eur J Neurosci 11:3276–3286. doi:10.1046/j.1460-9568.1999.00753.x
Blangero A, Ota H, Delporte L, Revol P, Vindras P, Rode G, Boisson D, Vighetto A, Rossetti Y, Pisella L (2007) Optic ataxia is not only ‘optic’: impaired spatial integration of proprioceptive information. Neuroimage 36:T61–T68. doi:10.1016/j.neuroimage.2007.03.039
Brown LE, Halpert BA, Goodale MA (2005) Peripheral vision for perception and action. Exp Brain Res 165:97–106. doi:10.1007/s00221-005-2285-y
Cavina-Pratesi C, Ietswaart M, Humphreys GW, Lestou V, Milner AD (2010a) Impaired grasping in a patient with optic ataxia: primary visuomotor deficit or secondary consequence of misreaching? Neuropsychologia 48:226–234. doi:10.1016/j.neuropsychologia.2009.09.008
Cavina-Pratesi C, Monaco S, Fattori P, Galletti C, McAdam TD, Quinlan DJ, Goodale MA, Culham JC (2010b) Functional magnetic resonance imaging reveals the neural substrates of arm transport and grip formation in reach-to-grasp actions in humans. J Neurosci 30:10306–10323. doi:10.1523/JNEUROSCI.2023-10.2010
Clavagnier S, Prado J, Kennedy H, Perenin MT (2007) How humans reach: distinct cortical systems for central and peripheral vision. Neuroscientist 13:22–27. doi:10.1177/1073858406295688
de Bruin N, Sacrey LA, 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 Mot Behav 40:337–346. doi:10.3200/JMBR.40.4.337-346
Dijkerman HC, de Haan EHF (2007) Somatosensory processes subserving perception and action. Behav Brain Sci 30:189–239. doi:10.1017/S0140525X07001392
Edwards MG, Wing AM, Stevens J, Humphreys GW (2005) Knowing your nose better than your thumb: measures of over-grasp reveal that face-parts are special for grasping. Exp Brain Res 161:72–80. doi:10.1007/s00221-004-2047-2
Fiehler K, Rosler F (2010) Plasticity of multisensory dorsal stream functions: evidence from congenitally blind and sighted adults. Restor Neurol Neurosci 28:193–205. doi:10.3233/RNN-2010-0500
Fiehler K, Burke M, Bien S, Roder B, Rosler F (2009) The human dorsal action control system develops in the absence of vision. Cereb Cortex 19:1–12. doi:10.1093/cercor/bhn067
Gharbawie OA, Stepniewska I, Kaas JH (2011) Cortical connections of functional zones in posterior parietal cortex and frontal cortex motor regions in new world monkeys. Cereb Cortex 21:1981–2002. doi:10.1093/cercor/bhq260
Gonzalez CL, Ganel T, Whitwell RL, Morrissey B, Goodale MA (2008) Practice makes perfect, but only with the right hand: sensitivity to perceptual illusions with awkward grasps decreases with practice in the right but not the left hand. Neuropsychologia 46:624–631. doi:10.1016/j.neuropsychologia.2007.09.006
Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15:20–25. doi:10.1016/0166-2236(92)90344-8
Hu Y, Eagleson R, Goodale MA (1999) The effects of delay on the kinematics of grasping. Exp Brain Res 126:109–116. doi:10.1007/s002210050720
Jakobson LS, Goodale MA (1991) Factors affecting higher-order movement planning: a kinematic analysis of human prehension. Exp Brain Res 86:199–208. doi:10.1007/BF00231054
Jackson SR, Newport R, Husain M, Fowlie JE, O'Donoghue M, Bajaj N (2009) There may be more to reaching than meets the eye: re-thinking optic ataxia. Neuropsychologia 47:1397-1408. doi:10.1016/j.neuropsychologia.2009.01.035
Jeannerod M (1999) Visuomotor channels: their integration in goal-directed prehension. Hum Mov Sci 18:201–218. doi:10.1016/S0167-9457(99)00008-1
Jeannerod M, Arbib MA, Rizzolatti G, Sakata H (1995) Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18:314–320. doi:10.1016/0166-2236(95)93921-J
Karl JM, Whishaw IQ (2013) Different evolutionary origins for the reach and the grasp: an explanation for dual visuomotor channels in primate parietofrontal cortex. Front Neurol 4:208. doi:10.3389/fneur.2013.00208
Karl JM, Sacrey LA, Doan JB, Whishaw IQ (2012a) Hand shaping using hapsis resembles visually guided hand shaping. Exp Brain Res 219:59–74. doi:10.1007/s00221-012-3067-y
Karl JM, Sacrey LA, Doan JB, Whishaw IQ (2012b) Oral hapsis guides accurate hand preshaping for grasping food targets in the mouth. Exp Brain Res 221:223–240. doi:10.1007/s00221-012-3164-y
Karl JM, Schneider LR, Whishaw IQ (2013) Nonvisual learning of intrinsic object properties in a reaching task dissociates grasp from reach. Exp Brain Res 225:465–477. doi:10.1007/s00221-012-3386-z
Karnath HO, Perenin MT (2005) Cortical control of visually guided reaching: evidence from patients with optic ataxia. Cereb Cortex 15:1561–1569. doi:10.1093/cercor/bhi034
Loftus A, Servos P, Goodale MA, Mendarozqueta N, Mon-Williams M (2004) When two eyes are better than one in prehension: monocular viewing and end-point variance. Exp Brain Res 158:317–327. doi:10.1007/s00221-004-1905-2
Ludwig CJ, Davies JR, Eckstein MP (2014) Foveal analysis and peripheral selection during active visual sampling. Proc Natl Acad Sci USA 111(2):E291–E299. doi:10.1073/pnas.1313553111
Milner AD, Goodale MA (2006) The visual brain in action, 2nd edn. Oxford University, Oxford
Pellegrino JW, Klatzky RL, McCloskey BP (1989) Time course of preshaping for functional responses to objects. J Mot Behav 21:307–316. doi:10.1080/00222895.1989.10735484
Perenin MT, Vighetto A (1988) Optic ataxia: a specific disruption in visuomotor mechanisms. I. Different aspects of the deficit in reaching for objects. Brain 111:643–674. doi:10.1093/brain/111.3.643
Pettypiece CE, Goodale MA, Culham JC (2010) Integration of haptic and visual size cues in perception and action revealed through cross-modal conflict. Exp Brain Res 201:863–873. doi:10.1007/s00221-009-2101-1
Prablanc C, Echallier JF, Komilis E, Jeannerod M (1979) Optimal response of eye and hand motor systems in pointing at a visual target. I. Spatio-temporal characteristics of eye and hand movements and their relationships when varying the amount of visual information. Biol Cybern 35:113–124. doi:10.1007/BF00337436
Prado J, Clavagnier S, Otzenberger H, Scheiber C, Kennedy H, Perenin MT (2005) Two cortical systems for reaching in central and peripheral vision. Neuron 48:849–858. doi:10.1016/j.neuron.2005.10.010
Rizzolatti G, Luppino G, Matelli M (1998) The organization of the cortical motor system: new concepts. Electroencephalogr Clin Neurophysiol 106:283–296. doi:10.1016/S0013-4694(98)00022-4
Sacrey LA, Whishaw IQ (2012) Subsystems of sensory attention for skilled reaching: vision for transport and pre-shaping and somatosensation for grasping, withdrawal and release. Behav Brain Res 231:356–365. doi:10.1016/j.bbr.2011.07.031
Sartori L, Staulino E, Castiello U (2011) How objects are grasped: the interplay between affordances and end-goals. PLoS One 6:e25203. doi:10.1371/journal.pone.0025203
Schlicht EJ, Schrater PR (2003) Bayesian model for reaching and grasping peripheral and occluded targets. J Vis 3:261a. doi:10.1167/3.9.261
Schlicht EJ, Schrater PR (2007) Effects of visual uncertainty on grasping movements. Exp Brain Res 182:47–57. doi:10.1007/s00221-007-0970-8
Schmidt J, Berg DR, Ploeg HL, Pleog L (2009) Precision, repeatability and accuracy of Optotrak optical motion tracking systems. Int J Exp Comput Biomech 1:114–127. doi:10.1504/IJECB.2009.022862
Sivak B, MacKenzie CL (1990) Integration of visual information and motor output in reaching and grasping: the contributions of peripheral and central vision. Neuropsychologia 28:1095–1116. doi:10.1016/0028-3932(90)90143-C
Tanne-Gariepy J, Rouiller EM, Boussaoud D (2002) Parietal inputs to dorsal versus ventral premotor areas in the macaque monkey: evidence for largely segregated visuomotor pathways. Exp Brain Res 145:91–103. doi:10.1007/s00221-002-1078-9
Thompson AA, Byrne PA, Henriques DY (2014) Visual targets aren’t irreversibly converted to motor coordinates: eye-centered updating of visuospatial memory in online reach control. PLoS One 9:e92455. doi:10.1371/journal.pone.0092455
Thorpe SJ, Gegenfurtner KR, Fabre-Thorpe M, Bülthoff HH (2001) Detection of animals in natural images using far peripheral vision. Eur J Neurosci 14:869–876. doi:10.1046/j.0953-816x.2001.01717.x
Valyear KF, Chapman CS, Gallivan JP, Mark RS, Culham JC (2011) To use or to move: goal-set modulates priming when grasping real tools. Exp Brain Res 212:125–142. doi:10.1007/s00221-011-2705-0
Vesia M, Bolton DA, Mochizuki G, Staines WR (2013) Human parietal and primary motor cortical interactions are selectively modulated during the transport and grip formation of goal-directed hand actions. Neuropsychologia 51:410–417. doi:10.1016/j.neuropsychologia.2012.11.022
Acknowledgments
The authors would like to thank Emilyne S. Jankunis for help with figure preparation, Layne A. Lenhart for help with data collection, and two anonymous reviewers for helpful comments on a previous draft of this paper. This research was supported by the Natural Sciences and Engineering Research Council of Canada (JMK, IQW), Alberta Innovates-Health Solutions (JMK), and Canadian Institutes of Health Research (IQW).
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Grasping strategies with vision, without vision, and with peripheral vision (45°). Filmed at 300 frames/second and played back at 30 frames/second (MOV 23817 kb)
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Hall, L.A., Karl, J.M., Thomas, B.L. et al. Reach and Grasp reconfigurations reveal that proprioception assists reaching and hapsis assists grasping in peripheral vision. Exp Brain Res 232, 2807–2819 (2014). https://doi.org/10.1007/s00221-014-3945-6
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DOI: https://doi.org/10.1007/s00221-014-3945-6