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Sensory integration during reaching: the effects of manipulating visual target availability

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Abstract

When using visual and proprioceptive information to plan a reach, it has been proposed that the brain combines these cues to estimate the object and/or limb’s location. Specifically, according to the maximum-likelihood estimation (MLE) model, sensory inputs are combined such that more reliable inputs are assigned a greater weight (Ernst and Banks in Nature 415:429–433, 2002). In this paper, we examined if the brain is able to adjust which sensory cue it weights the most. Specifically, we asked if the brain changes how it weights sensory information when the availability of a visual cue is manipulated. Twelve healthy subjects reached to visual (V), proprioceptive (P), or visual + proprioceptive (VP) targets under different visual delay conditions (e.g., on V and VP trials, the visual target was available for the entire reach; it was removed with the go signal, or it was removed 1 s before the go signal). To establish which sensory cue subjects weighted the most, we compared endpoint positions achieved on V and P reaches to VP reaches. Results indicated that subjects combined visual and proprioceptive cues in accordance with the MLE model when reaching to VP targets. Moreover, subjects’ reaching errors to visual targets increased with longer visual delays (particularly in the vertical direction). However, there was no change in reach variability with longer delays, and subjects did not reweight visual information as the availability of visual information was manipulated. Thus, a change in visual environment is not sufficient to cause the brain to reweight how it processes sensory information.

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References

  • Amedi A, Malach R, Hendler T, Peled S, Zohary E (2001) Visuo-haptic object-related activation in the ventral visual pathway. Nat Neurosci 4:324–330

    Article  CAS  PubMed  Google Scholar 

  • Berkinblit M, Fookson O, Smetanin B, Adamovich S, Poizner H (1995) The interaction of visual and proprioceptive inputs in pointing to actual and remembered targets. Exp Brain Res 107:326–330

    Article  CAS  PubMed  Google Scholar 

  • Block H, Bastian A (2010) Sensory reweighting in targeted reaching: effects of conscious effort, error history, and target salience. J Neurophysiol 103:206–217

    Article  PubMed Central  PubMed  Google Scholar 

  • Block H, Bastian A (2011) Sensory weighting and realignment: independent compensatory processes. J Neurophysiol 106:59–70

    Article  PubMed Central  PubMed  Google Scholar 

  • Block H, Bastian A (2012) Cerebellar involvement in motor but not sensory adaptation. Neuropsychologia 50(8):1766–1775

    Article  PubMed Central  PubMed  Google Scholar 

  • Buneo CA, Jarvis MR, Batista AP, Andersen RA (2002) Direct visuomotor transformations for reaching. Nature 416:632–636

    Article  CAS  PubMed  Google Scholar 

  • Burns J, Blohm G (2010). Multi-sensory weights depend on contextual noise in reference frame transformations. Front Hum Neurosci 4, Article 221

  • Chapman C, Heath M, Westwood D, Roy E (2001) Memory for kinesthetically defined target location: evidence for manual asymmetries. Brain Cogn 46(1–2):62–66

    Article  CAS  PubMed  Google Scholar 

  • Churchland M, Afshar A, Shenoy K (2006) A central source of movement variability. Neuron 52:1085–1096

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Craske B, Crawshaw M (1975) Shifts in kinesthesis through time and after active passive movement. Percept Mot Skills 40:755–761

    Article  CAS  PubMed  Google Scholar 

  • Desmurget M, Vindras P, Gréa H, Viviani P, Grafton S (2000) Proprioception does not quickly drift during visual occlusion. Exp Brain Res 134:363–377

    Article  CAS  PubMed  Google Scholar 

  • Elliot D, Madalena J (1987) The influence of premovement visual information on manual aiming. Q J Exp Psychol 39(A):541–559

  • Ernst M, Banks M (2002) Humans integrate visual and haptic information in a statistically optimal fashion. Nature 415:429–433

    Article  CAS  PubMed  Google Scholar 

  • Ernst M, Bulthoff H (2004) Merging the senses into robust percept. Trends Cogn Sci 8(4):162–169

    Article  PubMed  Google Scholar 

  • Foxe J, Wylie G, Martinez A, Schroeder C, Javitt D, Guilfoyle D, Ritter W, Murray M (2002) Auditory-somatosensory multisensory processing in auditory association cortex: an fMRI study. J Neurophysiol 88:540–543

    PubMed  Google Scholar 

  • Gentile G, Petkova V, Ehrsson H (2011) Integration of visual and tactile signals from the hand in the human brain: an fMRI study. J Neurophysiol 105:910–922

    Article  PubMed Central  PubMed  Google Scholar 

  • Ghahramani Z, Wolpert D, Jordan M (1997) Computational models of sensorimotor integration. Adv Psychol 119:117–147

    Article  Google Scholar 

  • Goodale M, Milner A (1992) Separate visual pathways for perception and action. Trends Neurosci 15(1):20–25

    Article  CAS  PubMed  Google Scholar 

  • Goodale M, Jakobson L, Keillor J (1994) Differences in the visual control of pantomimed and natural grasping movements. Neuropsychologia 32:1159–1178

    Article  CAS  PubMed  Google Scholar 

  • Goodale M, Westwood D, Milner A (2004) Two distinct modes of control for object-directed action. Prog Brain Res 144:131–144

    Article  PubMed  Google Scholar 

  • Gordon J, Gilhardi M, Cooper S, Ghez C (1994) Accuracy of planar reaching movements. II. Systematic errors resulting from inertial anisotropy. Exp Brain Res 99:112–130

    Article  CAS  PubMed  Google Scholar 

  • Grefkes C, Weiss H, Zilles K, Fink R (2002) Crossmodal processing of object features in human anterior intraparietal cortex: an fMRI study implies equivalencies between humans and monkeys. Neuron 35:173–184

    Article  CAS  PubMed  Google Scholar 

  • Harris C, Wolpert D (1998) Signal-dependent noise determines motor planning. Nature 394:20

    Article  Google Scholar 

  • Heath M, Westwood D, Binsted G (2004) The control of memory-guided reaching movements in peripersonal space. Mot Control 8:76–106

    Google Scholar 

  • Helbig H, Ernst M (2007) Optimal integration of shape information from vision and touch. Exp Brain Res 179:595–606

    Article  PubMed  Google Scholar 

  • James T, Humphrey G, Gati J, Servos P, Menon R, Goodale M (2002) Haptic study of three-dimensional objects activates extrastriate visual areas. Neuropsychologia 40:1706–1714

    Article  PubMed  Google Scholar 

  • Jones S, Fiehler K, Henriques D (2012) A task-dependent effect of memory and hand-target on proprioceptive location. Neuropsychologia 50(7):1462–1470

    Article  PubMed  Google Scholar 

  • Kröger B, Kopp S, Lowit A (2009) A model for production, perception, and acquisition of actions in face-to-face communication. Cogn Process 11:187–205

    Article  PubMed  Google Scholar 

  • Martuzzi R, Murray M, Michel C, Thiran JP, Maeder P, Clarke S, Meuli R (2007) Multisensory interactions within human primary cortices revealed by BOLD dynamics. Cereb Cortex 17:1672–1679

    Article  PubMed  Google Scholar 

  • McIntyre J, Stratta F, Lacquaniti F (1997) Viewer-centered frame of reference for pointing to memorized targets in three-dimensional space. J Neurophysiol 78:1601–1618

    CAS  PubMed  Google Scholar 

  • McIntyre J, Stratta F, Droulez J, Lacquaniti F (2000) Analysis of pointing errors reveals properties of data representations and coordinate transformations within the central nervous system. Neural Comput 12(12):2823–2855

    Article  CAS  PubMed  Google Scholar 

  • Meyer D, Abrams R, Kornblum S, Wright C, Smith J (1988) Optimality in human motor performance: ideal control of rapid aimed movements. Psychol Rev 95(3):340–370

    Article  CAS  PubMed  Google Scholar 

  • Milner A, Paulignan Y, Dijkerman H, Michel F, Jeannerod M (1999) A paradoxical improvement of misreaching in optic ataxia: new evidence for two separate neural systems for visual localization. Proc R Soc Lond Ser B Biol Sci 266:2225–2229

    Article  CAS  Google Scholar 

  • Molholm S, Ritter W, Murrary M, Javitt D, Schroeher C, Foxe J (2002) Multisensory auditory–visual interactions during early sensory processing in humans: a high-density electrical mapping study. Brain Res Cogn Brain Res 14:115–128

    Article  PubMed  Google Scholar 

  • Monaco S, Kroliczak G, Quinlan D, Fattori P, Galletti C, Goddale M, Culham J (2010) Contribution of visual and proprioceptive information to the precision of reaching movements. Exp Brain Res 202:15–32

    Article  PubMed  Google Scholar 

  • Mon-Williams M, Wann J, Jenkinson M, Rushton K (1997) Synaesthesia in the normal limb. Proc R Soc Lond Ser B Biol Sci 264(1384):1007–1010

    Article  CAS  Google Scholar 

  • Naumer M, Ratz L, Yalachkov Y, Polony A, Doehrmann O, van de Ven V, Muller N, Kaiser J, Hein G (2010) Visuohaptic convergence in a corticocerebellar network. Eur J Neurosci 31:1730–1736

    Article  PubMed  Google Scholar 

  • Oldfield R (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychololgia 9:97–113

    Article  CAS  Google Scholar 

  • Pekkola J, Ojanen V, Autti T, Jaaskelainen I, Mottonen R, Tarkiainen A, Sams M (2005) Primary auditory cortex activation by visual speech: an fMRI study at 3 T. NeuroReport 16:125–128

    Article  PubMed  Google Scholar 

  • Reuschel J, Drewing K, Henriques D, Rosler F, Fiehler K (2010) Optimal integration of visual and proprioceptive movement information for the perception of trajectory geometry. Exp Brain Res 201:853–862

    Article  PubMed  Google Scholar 

  • Rossetti Y (1998) Implicit short-lived motor representations of space in brain damaged and healthy subjects. Conscious Cogn 7:520–558

    Article  CAS  PubMed  Google Scholar 

  • Saito D, Okada T, Morita Y, Yonekura Y, Sadato N (2003) Tactile-visual cross-modal shape matching: a functional MRI study. Cogn Brain Res 17:14–25

    Article  Google Scholar 

  • Sarlegna F, Sainburg R (2007) The effect of target modality on visual and proprioceptive contributions to the control of movement distance. Exp Brain Res 176:267–280

    Article  PubMed  Google Scholar 

  • Schmidt R, Zelaznik H, Hawkins B, Frank J, Quinn J (1979) Motor-output variability: a theory for the accuracy of rapid motor acts. Psychol Rev 86(5):415–451

    Article  Google Scholar 

  • Smeets J, van Den Dobbelsteen J, De Grave D, van Beers R, Brenner E (2006) Sensory integration does not lead to sensory calibration. Proc Natl Acad Sci USA 103(49):18781–18786

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sober S, Sabes P (2005) Flexible strategies for sensory integration during motor planning. Nat Neurosci 8(4):490–497

    CAS  PubMed Central  PubMed  Google Scholar 

  • Soechting J, Flanders M (1989) Sensorimotor representations for pointing to targets in three-dimensional space. J Neurophysiol 62(2):582–594

    CAS  PubMed  Google Scholar 

  • van Beers R (2009) Motor learning is optimally tuned to the properties of motor noise. Neuron 63:406–417

    Article  PubMed  Google Scholar 

  • van Beers R, Sitting A, van Der Gon D (1996) How humans combine simultaneous proprioceptive and visual position information. Exp Brain Res 111:253–261

    Article  PubMed  Google Scholar 

  • van Beers R, Sitting A, van Der Gon J (1998) The precision of proprioceptive position sense. Exp Brain Res 122:367–377

    Article  PubMed  Google Scholar 

  • van Beers R, Sitting A, van Der Gon D (1999) Integration of proprioceptive and visual position-information: an experimentally supported model. J Neurophysiol 81:1355–1364

    PubMed  Google Scholar 

  • van Beers R, Wolpert D, Haggard P (2002) When feeling is more important than seeing in sensorimotor adaptation. Curr Biol 12:834–837

    Article  PubMed  Google Scholar 

  • van Beers R, Haggard P, Wolpert D (2004) The role of execution noise in movement variability. J Neurophysiol 91:1050–1063

    Article  PubMed  Google Scholar 

  • van den Dobbelsteen J, Brenner E, Smeets J (2001) Endpoints of arm movements to visual targets. Exp Brain Res 138:279–287

    Article  PubMed  Google Scholar 

  • van Galen G, de Jong W (1995) Fitts’ law as the outcome of a dynamic noise filtering model of motor control. Hum Mov Sci 14:539–571

    Article  Google Scholar 

  • Vindras P, Viviani P (1998) Frames of reference and control parameters in visuomanual pointing. J Exp Psychol Hum Percept Perform 24(2):569–591

    Article  CAS  PubMed  Google Scholar 

  • Wann J, Ibrahim S (1992) Does limb proprioception drift? Exp Brain Res 91:162–166

    Article  CAS  PubMed  Google Scholar 

  • Warren D, Schmitt T (1978) On the plasticity of visual-proprioceptive bias effects. J Exp Psychol Hum Percept Perform 4(2):302–310

    Article  CAS  PubMed  Google Scholar 

  • Westwood D, Goodale M (2003) Perceptual illusion and the realtime control of action. Spat Vis 16:243–254

    Article  PubMed  Google Scholar 

  • Westwood D, Health M, Roy E (2001) The accuracy of reaching movements in brief delay conditions. Can J Exp Psychol 55(4):304–310

    Article  CAS  PubMed  Google Scholar 

  • Westwood D, Roy E, Health M (2003) No evidence for accurate visuomotor memory: systematic and variable error in memory-guided reaching. J Mot Behav 35(2):127–133

    Article  PubMed  Google Scholar 

  • Wong J, Wilson E, Kistemaker D, Gribble P (2014) Bimanual proprioception: are two hands better than one? J Neurophysiol 111(6):1362–1368

    Article  PubMed  Google Scholar 

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  1. School of Human Kinetics, University of Ottawa, 125 University Private, Ottawa, ON, K1N 6N5, Canada

    Sajida Khanafer & Erin K. Cressman

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  1. Sajida Khanafer
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  2. Erin K. Cressman
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Correspondence to Sajida Khanafer.

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Khanafer, S., Cressman, E.K. Sensory integration during reaching: the effects of manipulating visual target availability. Exp Brain Res 232, 3833–3846 (2014). https://doi.org/10.1007/s00221-014-4064-0

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