Abstract

Sensory processing in the brain includes three key operations: multisensory integration—the task of combining cues into a single estimate of a common underlying stimulus; coordinate transformations—the change of reference frame for a stimulus (e.g., retinotopic to body-centered) effected through knowledge about an intervening variable (e.g., gaze position); and the incorporation of prior information. Statistically optimal sensory processing requires that each of these operations maintains the correct posterior distribution over the stimulus. Elements of this optimality have been demonstrated in many behavioral contexts in humans and other animals, suggesting that the neural computations are indeed optimal. That the relationships between sensory modalities are complex and plastic further suggests that these computations are learned—but how? We provide a principled answer, by treating the acquisition of these mappings as a case of density estimation, a well-studied problem in machine learning and statistics, in which the distribution of observed data is modeled in terms of a set of fixed parameters and a set of latent variables. In our case, the observed data are unisensory-population activities, the fixed parameters are synaptic connections, and the latent variables are multisensory-population activities. In particular, we train a restricted Boltzmann machine with the biologically plausible contrastive-divergence rule to learn a range of neural computations not previously demonstrated under a single approach: optimal integration; encoding of priors; hierarchical integration of cues; learning when not to integrate; and coordinate transformation. The model makes testable predictions about the nature of multisensory representations.

Highlights

  • The brain often receives information about the same feature of the same object from multiple sources; e.g., in a visually guided reach, both vision and proprioception provide information about hand location

  • Prism and virtualfeedback adapation experiments [8,9,10,11,12] have demonstrated the plasticity of these multisensory mappings, and it is not likely limited to recalibration: Deprivation studies [13]; afferent rerouting experiments [14,15]; the ability to learn novel, cross-modal mappings; and genetic-information constraints together suggest that integration is learned, with the organization of association cortices driven by sensory data

  • We present a biologically plausible artificial neural network that learns all of the above in just this way, but by training it for a much more general statistical task: ‘‘density estimation’’—essentially, learning to be able to reproduce the data on which it was trained

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Summary

Introduction

The brain often receives information about the same feature of the same object from multiple sources; e.g., in a visually guided reach, both vision and proprioception provide information about hand location. Were both signals infinitely precise, one could be ignored; but fidelity is limited by irrelevant inputs, intrinsic neural noise, and the spatial precisions of the transducers, so there are better and worse ways to use them. Encoding in the integrating neurons the entire posterior for each stimulus, and not merely the best point estimate, is crucial because this distribution contains information about the confidence of the estimate, which is required for optimal computation with the stimulus estimate [1,2]. Prism and virtualfeedback adapation experiments [8,9,10,11,12] have demonstrated the plasticity of these multisensory mappings, and it is not likely limited to recalibration: Deprivation studies [13]; afferent rerouting experiments [14,15]; the ability to learn novel, cross-modal mappings; and genetic-information constraints together suggest that integration is learned, with the organization of association cortices driven by sensory data

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