A neural surveyor to map touch on the body.

Journal: Proceedings of the National Academy of Sciences of the United States of America
Published Date:

Abstract

Perhaps the most recognizable sensory map in all of neuroscience is the somatosensory homunculus. Although it seems straightforward, this simple representation belies the complex link between an activation in a somatotopic map and the associated touch location on the body. Any isolated activation is spatially ambiguous without a neural decoder that can read its position within the entire map, but how this is computed by neural networks is unknown. We propose that the somatosensory system implements multilateration, a common computation used by surveying and global positioning systems to localize objects. Specifically, to decode touch location on the body, multilateration estimates the relative distance between the afferent input and the boundaries of a body part (e.g., the joints of a limb). We show that a simple feedforward neural network, which captures several fundamental receptive field properties of cortical somatosensory neurons, can implement a Bayes-optimal multilateral computation. Simulations demonstrated that this decoder produced a pattern of localization variability between two boundaries that was unique to multilateration. Finally, we identify this computational signature of multilateration in actual psychophysical experiments, suggesting that it is a candidate computational mechanism underlying tactile localization.

Authors

  • Luke E Miller
    Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen 6500 GL, The Netherlands; Luke.Miller@donders.ru.nl.
  • Cécile Fabio
    Integrative Multisensory Perception Action and Cognition Team - ImpAct, Lyon Neuroscience Research Center, INSERM U1028, CNRS U5292, Bron 69500, France.
  • Malika Azaroual
    Integrative Multisensory Perception Action and Cognition Team - ImpAct, Lyon Neuroscience Research Center, INSERM U1028, CNRS U5292, Bron 69500, France.
  • Dollyane Muret
    Institute of Cognitive Neuroscience, University College London, London WC1N 3AZ, United Kingdom.
  • Robert J van Beers
    Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen 6500 GL, The Netherlands.
  • Alessandro Farnè
    Integrative Multisensory Perception Action and Cognition Team - ImpAct, Lyon Neuroscience Research Center, INSERM U1028, CNRS U5292, Bron 69500, France.
  • W Pieter Medendorp
    Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen 6500 GL, The Netherlands.