Abstract
The sensory signals that drive movement planning arrive in a variety of 'reference frames', and integrating or comparing them requires sensory transformations. We propose a model in which the statistical properties of sensory signals and their transformations determine how these signals are used. This model incorporates the patterns of gaze-dependent errors that we found in our human psychophysics experiment when the sensory signals available for reach planning were varied. These results challenge the widely held ideas that error patterns directly reflect the reference frame of the underlying neural representation and that it is preferable to use a single common reference frame for movement planning. We found that gaze-dependent error patterns, often cited as evidence for retinotopic reach planning, can be explained by a transformation bias and are not exclusively linked to retinotopic representations. Furthermore, the presence of multiple reference frames allows for optimal use of available sensory information and explains task-dependent reweighting of sensory signals.
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References
Schlicht, E.J. & Schrater, P.R. Impact of coordinate transformation uncertainty on human sensorimotor control. J. Neurophysiol. 97, 4203–4214 (2007).
Sober, S.J. & Sabes, P.N. Flexible strategies for sensory integration during motor planning. Nat. Neurosci. 8, 490–497 (2005).
Buneo, C.A. & Andersen, R.A. The posterior parietal cortex: sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia 44, 2594–2606 (2006).
Cohen, Y.E. & Andersen, R.A. A common reference frame for movement plans in the posterior parietal cortex. Nat. Rev. Neurosci. 3, 553–562 (2002).
Engel, K.C., Flanders, M. & Soechting, J.F. Oculocentric frames of reference for limb movement. Arch. Ital. Biol. 140, 211–219 (2002).
Lacquaniti, F. & Caminiti, R. Visuo-motor transformations for arm reaching. Eur. J. Neurosci. 10, 195–203 (1998).
Soechting, J.F. & Flanders, M. Sensorimotor representations for pointing to targets in three-dimensional space. J. Neurophysiol. 62, 582–594 (1989).
Beurze, S.M., Van Pelt, S. & Medendorp, W.P. Behavioral reference frames for planning human reaching movements. J. Neurophysiol. 96, 352–362 (2006).
Henriques, D.Y., Klier, E.M., Smith, M.A., Lowy, D. & Crawford, J.D. Gaze-centered remapping of remembered visual space in an open-loop pointing task. J. Neurosci. 18, 1583–1594 (1998).
Pouget, A., Ducom, J.C., Torri, J. & Bavelier, D. Multisensory spatial representations in eye-centered coordinates for reaching. Cognition 83, B1–B11 (2002).
McIntyre, J., Stratta, F. & Lacquaniti, F. Viewer-centered frame of reference for pointing to memorized targets in three-dimensional space. J. Neurophysiol. 78, 1601–1618 (1997).
Carrozzo, M., McIntyre, J., Zago, M. & Lacquaniti, F. Viewer-centered and body-centered frames of reference in direct visuomotor transformations. Exp. Brain Res. 129, 201–210 (1999).
McIntyre, J., Stratta, F. & Lacquaniti, F. Short-term memory for reaching to visual targets: psychophysical evidence for body-centered reference frames. J. Neurosci. 18, 8423–8435 (1998).
Avillac, M., Deneve, S., Olivier, E., Pouget, A. & Duhamel, J.R. Reference frames for representing visual and tactile locations in parietal cortex. Nat. Neurosci. 8, 941–949 (2005).
Batista, A.P., Buneo, C.A., Snyder, L.H. & Andersen, R.A. Reach plans in eye-centered coordinates. Science 285, 257–260 (1999).
Batista, A.P. et al. Reference frames for reach planning in macaque dorsal premotor cortex. J. Neurophysiol. 98, 966–983 (2007).
Battaglia-Mayer, A. et al. Eye-hand coordination during reaching. II. An analysis of the relationships between visuomanual signals in parietal cortex and parieto-frontal association projections. Cereb. Cortex 11, 528–544 (2001).
Buneo, C.A., Jarvis, M.R., Batista, A.P. & Andersen, R.A. Direct visuomotor transformations for reaching. Nature 416, 632–636 (2002).
Lacquaniti, F., Guigon, E., Bianchi, L., Ferraina, S. & Caminiti, R. Representing spatial information for limb movement: role of area 5 in the monkey. Cereb. Cortex 5, 391–409 (1995).
Medendorp, W.P., Goltz, H.C., Vilis, T. & Crawford, J.D. Gaze-centered updating of visual space in human parietal cortex. J. Neurosci. 23, 6209–6214 (2003).
Pesaran, B., Nelson, M.J. & Andersen, R.A. Dorsal premotor neurons encode the relative position of the hand, eye and goal during reach planning. Neuron 51, 125–134 (2006).
Wu, W. & Hatsopoulos, N. Evidence against a single coordinate system representation in the motor cortex. Exp. Brain Res. 175, 197–210 (2006).
Wu, W. & Hatsopoulos, N.G. Coordinate system representations of movement direction in the premotor cortex. Exp. Brain Res. 176, 652–657 (2007).
Burnod, Y. et al. Parieto-frontal coding of reaching: an integrated framework. Exp. Brain Res. 129, 325–346 (1999).
Caminiti, R., Ferraina, S. & Mayer, A.B. Visuomotor transformations: early cortical mechanisms of reaching. Curr. Opin. Neurobiol. 8, 753–761 (1998).
Carrozzo, M. & Lacquaniti, F. A hybrid frame of reference for visuo-manual coordination. Neuroreport 5, 453–456 (1994).
Bock, O. Contribution of retinal versus extraretinal signals towards visual localization in goal-directed movements. Exp. Brain Res. 64, 476–482 (1986).
Knill, D.C. & Pouget, A. The Bayesian brain: the role of uncertainty in neural coding and computation. Trends Neurosci. 27, 712–719 (2004).
Blohm, G. & Crawford, J.D. Computations for geometrically accurate visually guided reaching in 3-D space. J. Vis. 7, 1–22 (2007).
van Beers, R.J., Sittig, A.C. & Denier van der Gon, J.J. The precision of proprioceptive position sense. Exp. Brain Res. 122, 367–377 (1998).
Land, M.F. & Hayhoe, M. In what ways do eye movements contribute to everyday activities? Vision Res. 41, 3559–3565 (2001).
Balslev, D. & Miall, R.C. Eye position representation in human anterior parietal cortex. J. Neurosci. 28, 8968–8972 (2008).
Van Pelt, S. & Medendorp, W.P. Updating target distance across eye movements in depth. J. Neurophysiol. 99, 2281–2290 (2008).
Ernst, M.O. & Banks, M.S. Humans integrate visual and haptic information in a statistically optimal fashion. Nature 415, 429–433 (2002).
Helbig, H.B. & Ernst, M.O. Optimal integration of shape information from vision and touch. Exp. Brain Res. 179, 595–606 (2007).
Kording, K.P. & Wolpert, D.M. Probabilistic mechanisms in sensorimotor control. Novartis Found. Symp. 270, 191–198; discussion 198–202, 232–197 (2006).
van Beers, R.J., Sittig, A.C. & Gon, J.J. Integration of proprioceptive and visual position-information: an experimentally supported model. J. Neurophysiol. 81, 1355–1364 (1999).
Yuille, A.L. & Bulthoff, H.H. Bayesian decision theory and psychophysics. in Perception as Bayesian Inference 123–136 (Cambridge University Press, Cambridge, UK, 1996).
Henriques, D.Y. & Crawford, J.D. Direction-dependent distortions of retinocentric space in the visuomotor transformation for pointing. Exp. Brain Res. 132, 179–194 (2000).
Henriques, D.Y. & Crawford, J.D. Role of eye, head and shoulder geometry in the planning of accurate arm movements. J. Neurophysiol. 87, 1677–1685 (2002).
Lewald, J. & Ehrenstein, W.H. Visual and proprioceptive shifts in perceived egocentric direction induced by eye position. Vision Res. 40, 539–547 (2000).
Vindras, P., Desmurget, M., Prablanc, C. & Viviani, P. Pointing errors reflect biases in the perception of the initial hand position. J. Neurophysiol. 79, 3290–3294 (1998).
Soechting, J.F. & Flanders, M. Errors in pointing are due to approximations in sensorimotor transformations. J. Neurophysiol. 62, 595–608 (1989).
Kording, K.P. & Tenenbaum, J.B. Causal inference in multisensory integration. in NIPS 737–744 (MIT Press, Cambridge, Massachusetts, 2006).
Ahmed, A.A., Wolpert, D.M. & Flanagan, J.R. Flexible representations of dynamics are used in object manipulation. Curr. Biol. 18, 763–768 (2008).
Kluzik, J., Diedrichsen, J., Shadmehr, R. & Bastian, A.J. Reach adaptation: what determines whether we learn an internal model of the tool or adapt the model of our arm? J. Neurophysiol. 100, 1455–1464 (2008).
Battaglia-Mayer, A., Caminiti, R., Lacquaniti, F. & Zago, M. Multiple levels of representation of reaching in the parieto-frontal network. Cereb. Cortex 13, 1009–1022 (2003).
Cohen, Y.E. & Andersen, R.A. Reaches to sounds encoded in an eye-centered reference frame. Neuron 27, 647–652 (2000).
Mullette-Gillman, O.A., Cohen, Y.E. & Groh, J.M. Eye-centered, head-centered and complex coding of visual and auditory targets in the intraparietal sulcus. J. Neurophysiol. 94, 2331–2352 (2005).
Good, P.I. Permutation Tests: A Practical Guide to Resampling Methods for Testing Hypotheses, 2nd edn. (Springer-Verlag, New York, 2000).
Acknowledgements
We would like to thank S.M. Beurze, S. van Pelt, W.P. Medendorp and S.J. Sober for generously providing their data for model comparison. This work was supported by the National Eye Institute (R01 EY-015679), the National Institute of Mental Health (P50 MH77970) and the McKnight Endowment Fund for Neuroscience. L.M.M.M. was supported by a graduate fellowship from the National Science Foundation.
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McGuire, L., Sabes, P. Sensory transformations and the use of multiple reference frames for reach planning. Nat Neurosci 12, 1056–1061 (2009). https://doi.org/10.1038/nn.2357
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DOI: https://doi.org/10.1038/nn.2357
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