Abstract

The challenge of building increasingly better models of neural responses to natural stimuli is to accurately estimate the multiple stimulus features that may jointly affect the neural spike probability. The selectivity for combinations of features is thought to be crucial for achieving classical properties of neural responses such as contrast invariance. The joint search for these multiple stimulus features is difficult because estimating spike probability as a multidimensional function of stimulus projections onto candidate relevant dimensions is subject to the curse of dimensionality. An attractive alternative is to search for relevant dimensions sequentially, as in projection pursuit regression. Here we demonstrate using analytic arguments and simulations of model cells that different types of sequential search strategies exhibit systematic biases when used with natural stimuli. Simulations show that joint optimization is feasible for up to three dimensions with current algorithms. When applied to the responses of V1 neurons to natural scenes, models based on three jointly optimized dimensions had better predictive power in a majority of cases compared to dimensions optimized sequentially, with different sequential methods yielding comparable results. Thus, although the curse of dimensionality remains, at least several relevant dimensions can be estimated by joint information maximization.

Highlights

  • An essential element for achieving a quantitative understanding of sensory processing consists of characterizing the computational rules according to which the incoming stimuli are encoded within the sensory pathways

  • The joint search for these multiple stimulus features is difficult because estimating spike probability as a multidimensional function of stimulus projections onto candidate relevant dimensions is subject to the curse of dimensionality

  • In agreement with theoretical arguments based on properties of the gradient (Equation (11)), we found that in the case of noise stimuli, the two relevant dimensions could be correctly reconstructed with a sequential search (Figure 1B)

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Summary

Introduction

ISSN 0954-898X print/ISSN 1361-6536 online/01/01-0400045–73 ß 2011 Informa Healthcare Ltd. In the case of neural responses to noise inputs, sequential and joint optimization of relevant dimensions produced comparable results (the small difference in predictive power is likely due to small non-Gaussian effects introduced during the discretization of intensity levels). The percent information explained on a novel dataset was 63 Æ 3% for the sequential search and 90 Æ 4% for the joint search These simulations illustrate that the non-Gaussian correlations in natural stimuli are strong enough to qualitatively and quantitatively alter results of the sequential optimization away from the true (model) relevant dimensions. The nonlinear gain functions computed with respect to the reconstructed dimensions yielded dependencies that were in agreement with the model, taking into account that the reconstructed dimensions represent linear combinations of model dimensions This demonstrates that the joint information maximization can estimate up to three relevant dimensions. Analysis of the predictive power across the population of V1 cells is consistent with the conclusion that the reconstruction of relevant dimensions from neural responses to natural stimuli requires their joint optimization

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