The efficient coding hypothesis assumes that biological sensory systems use neural codes that are optimized to best possibly represent the stimuli that occur in their environment. Most common models use information–theoretic measures, whereas alternative formulations propose incorporating downstream decoding performance. Here we provide a systematic evaluation of different optimality criteria using a parametric formulation of the efficient coding problem based on the reconstruction error of the maximum likelihood decoder. This parametric family includes both the information maximization criterion and squared decoding error as special cases. We analytically derived the optimal tuning curve of a single neuron encoding a one-dimensional stimulus with an arbitrary input distribution. We show how the result can be generalized to a class of neural populations by introducing the concept of a meta–tuning curve. The predictions of our framework are tested against previously measured characteristics of some early visual systems found in biology. We find solutions that correspond to low values of , suggesting that across different animal models, neural representations in the early visual pathways optimize similar criteria about natural stimuli that are relatively close to the information maximization criterion.

Fisher information is generally believed to represent a lower bound on mutual information (Brunel & Nadal, 1998 ), a result that is frequently used in the assessment of neural coding efficiency. However, we demonstrate that the relation between these two quantities is more nuanced than previously thought. For example, we find that in the small noise regime, Fisher information actually provides an upper bound on mutual information. Generally our results show that it is more appropriate to consider Fisher information as an approximation rather than a bound on mutual information. We analytically derive the correspondence between the two quantities and the conditions under which the approximation is good. Our results have implications for neural coding theories and the link between neural population coding and psychophysically measurable behavior. Specifically, they allow us to formulate the efficient coding problem of maximizing mutual information between a stimulus variable and the response of a neural population in terms of Fisher information. We derive a signature of efficient coding expressed as the correspondence between the population Fisher information and the distribution of the stimulus variable. The signature is more general than previously proposed solutions that rely on specific assumptions about the neural tuning characteristics. We demonstrate that it can explain measured tuning characteristics of cortical neural populations that do not agree with previous models of efficient coding.

Neural activity and perception are both affected by sensory history. The work presented here explores the relationship between the physiological effects of adaptation and their perceptual consequences. Perception is modeled as arising from an encoder-decoder cascade, in which the encoder is defined by the probabilistic response of a population of neurons, and the decoder transforms this population activity into a perceptual estimate. Adaptation is assumed to produce changes in the encoder, and we examine the conditions under which the decoder behavior is consistent with observed perceptual effects in terms of both bias and discriminability. We show that for all decoders, discriminability is bounded from below by the inverse Fisher information. Estimation bias, on the other hand, can arise for a variety of different reasons and can range from zero to substantial. We specifically examine biases that arise when the decoder is fixed, “unaware” of the changes in the encoding population (as opposed to “aware” of the adaptation and changing accordingly). We simulate the effects of adaptation on two well-studied sensory attributes, motion direction and contrast, assuming a gain change description of encoder adaptation. Although we cannot uniquely constrain the source of decoder bias, we find for both motion and contrast that an “unaware” decoder that maximizes the likelihood of the percept given by the preadaptation encoder leads to predictions that are consistent with behavioral data. This model implies that adaptation-induced biases arise as a result of temporary suboptimality of the decoder.