A simple model of optimal population coding for sensory systems.

A fundamental task of a sensory system is to infer information about the environment. It has long been suggested that an important goal of the first stage of this process is to encode the raw sensory signal efficiently by reducing its redundancy in the neural representation. Some redundancy, however, would be expected because it can provide robustness to noise inherent in the system. Encoding the raw sensory signal itself is also problematic, because it contains distortion and noise. The optimal solution would be constrained further by limited biological resources. Here, we analyze a simple theoretical model that incorporates these key aspects of sensory coding, and apply it to conditions in the retina. The model specifies the optimal way to incorporate redundancy in a population of noisy neurons, while also optimally compensating for sensory distortion and noise. Importantly, it allows an arbitrary input-to-output cell ratio between sensory units (photoreceptors) and encoding units (retinal ganglion cells), providing predictions of retinal codes at different eccentricities. Compared to earlier models based on redundancy reduction, the proposed model conveys more information about the original signal. Interestingly, redundancy reduction can be near-optimal when the number of encoding units is limited, such as in the peripheral retina. We show that there exist multiple, equally-optimal solutions whose receptive field structure and organization vary significantly. Among these, the one which maximizes the spatial locality of the computation, but not the sparsity of either synaptic weights or neural responses, is consistent with known basic properties of retinal receptive fields. The model further predicts that receptive field structure changes less with light adaptation at higher input-to-output cell ratios, such as in the periphery.

Efficient coding of spatial information in the primate retina.

Sensory neurons have been hypothesized to efficiently encode signals from the natural environment subject to resource constraints. The predictions of this efficient coding hypothesis regarding the spatial filtering properties of the visual system have been found consistent with human perception, but they have not been compared directly with neural responses. Here, we analyze the information that retinal ganglion cells transmit to the brain about the spatial information in natural images subject to three resource constraints: the number of retinal ganglion cells, their total response variances, and their total synaptic strengths. We derive a model that optimizes the transmitted information and compare it directly with measurements of complete functional connectivity between cone photoreceptors and the four major types of ganglion cells in the primate retina, obtained at single-cell resolution. We find that the ganglion cell population exhibited 80% efficiency in transmitting spatial information relative to the model. Both the retina and the model exhibited high redundancy (~30%) among ganglion cells of the same cell type. A novel and unique prediction of efficient coding, the relationships between projection patterns of individual cones to all ganglion cells, was consistent with the observed projection patterns in the retina. These results indicate a high level of efficiency with near-optimal redundancy in visual signaling by the retina.

Characterization of minimum error linear coding with sensory and neural noise.

Robust coding has been proposed as a solution to the problem of minimizing decoding error in the presence of neural noise. Many real-world problems, however, have degradation in the input signal, not just in neural representations. This generalized problem is more relevant to biological sensory coding where internal noise arises from limited neural precision and external noise from distortion of sensory signal such as blurring and phototransduction noise. In this note, we show that the optimal linear encoder for this problem can be decomposed exactly into two serial processes that can be optimized separately. One is Wiener filtering, which optimally compensates for input degradation. The other is robust coding, which best uses the available representational capacity for signal transmission with a noisy population of linear neurons. We also present spectral analysis of the decomposition that characterizes how the reconstruction error is minimized under different input signal spectra, types and amounts of degradation, degrees of neural precision, and neural population sizes.

Cone selectivity derived from the responses of the retinal cone mosaic to natural scenes.

To achieve color vision, the brain has to process signals of the cones in the retinal photoreceptor mosaic in a cone-type-specific way. We investigated the possibility that cone-type-specific wiring is an adaptation to the statistics of the cone signals. We analyzed estimates of cone responses to natural scenes and found that there is sufficient information in the higher order statistics of L- and M-cone responses to distinguish between cones of different types, enabling unsupervised learning of cone-type specificity. This was not the case for a fourth cone type with spectral sensitivity between L and M cones, suggesting an explanation for the lack of strong tetrachromacy in heterozygous carriers of color deficiencies.

Robust coding over noisy overcomplete channels.

We address the problem of robust coding in which the signal information should be preserved in spite of intrinsic noise in the representation. We present a theoretical analysis for 1- and 2-D cases and characterize the optimal linear encoder and decoder in the mean-squared error sense. Our analysis allows for an arbitrary number of coding units, thus including both under- and over-complete representations, and provides insights into optimal coding strategies. In particular, we show how the form of the code adapts to the number of coding units and to different data and noise conditions in order to achieve robustness. We also present numerical solutions of robust coding for high-dimensional image data, demonstrating that these codes are substantially more robust than other linear image coding methods such as PCA, ICA, and wavelets.

Spatiochromatic receptive field properties derived from information-theoretic analyses of cone mosaic responses to natural scenes.

Neurons in the early stages of processing in the primate visual system efficiently encode natural scenes. In previous studies of the chromatic properties of natural images, the inputs were sampled on a regular array, with complete color information at every location. However, in the retina cone photoreceptors with different spectral sensitivities are arranged in a mosaic. We used an unsupervised neural network model to analyze the statistical structure of retinal cone mosaic responses to calibrated color natural images. The second-order statistical dependencies derived from the covariance matrix of the sensory signals were removed in the first stage of processing. These decorrelating filters were similar to type I receptive fields in parvo- or konio-cellular LGN in both spatial and chromatic characteristics. In the subsequent stage, the decorrelated signals were linearly transformed to make the output as statistically independent as possible, using independent component analysis. The independent component filters showed luminance selectivity with simple-cell-like receptive fields, or had strong color selectivity with large, often double-opponent, receptive fields, both of which were found in the primary visual cortex (V1). These results show that the "form" and "color" channels of the early visual system can be derived from the statistics of sensory signals.