Sparse coding is a powerful idea in computational neuroscience referring to the general principle that the cortex exploits the benefits of representing every stimulus by a small subset of neurons. Advantages of sparse coding include reduced dependencies, improved detection of co-activation of neurons, and a more efficient encoding of visual information. Computational models based on this principle have reproduced the main characteristics of simple cell receptive fields in the primary visual cortex (V1) when applied to natural images. However, direct tests on neural data of whether sparse coding is an optimization principle actively implemented in the brain have been inconclusive so far. Although a number of electrophysiological studies have reported high levels of sparseness in V1, these measurements were made in absolute terms and thus it is an open question whether the observed high sparseness indicates optimality or simply high stimulus selectivity. Moreover, most of the recordings have been performed in anesthetized animals, but it is not clear how these results generalize to the cell responses in the awake condition. To address this issue, we have focused on relative changes in sparseness. We analyzed neural data from ferret and rat V1 to verify two basic predictions of sparse coding: 1) Over learning, neural responses should become increasingly sparse, as the visual system adapts to the statistics of the environment. 2) An optimal sparse representation requires active competition between neurons that is realized by recurrent connections. Thus, as animals go from awake state to deep anesthesia, which is known to eliminate recurrent and top-down inputs, neural responses should become less sparse, since the neural interactions that support active sparsification of responses are disrupted. To test the first prediction empirically, we measured the sparseness of neural responses in awake ferret V1 to natural movies at various stages of development, from eye opening to adulthood. Contrary to the prediction of sparse coding, we found that the neural code does adapt to represent natural stimuli over development, but sparseness steadily decreases with age. In addition, we observed a general increase in dependencies among neural responses. We addressed the second prediction by analyzing neural responses to natural movies in rats that were either awake or under different levels of anesthesia ranging from light to very deep. Again, contrary to the prediction, sparseness of cortical cells increased with increasing levels of anesthesia. We controlled for reduced responsiveness of the direct feedforward connections under anesthesia, by using appropriate sparseness measures and by quantifying the signal- to-noise ratio across levels of anesthesia, which did not change significantly. These findings suggest that the representation in V1 is not actively optimized to maximize the sparseness of neural responses. A viable alternative is that the concept of efficient coding is implemented in the form of optimal statistical learning of parameters in an internal model of the environment.

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