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Recently, deep feedforward neural networks have achieved considerable success in modeling biological sensory processing, in terms of reproducing the input-output map of sensory neurons. However, such models raise profound questions about the very nature of explanation in neuroscience. Are we simply replacing one complex system (a biological circuit) with another (a deep network), without understanding either? Moreover, beyond neural representations, are the deep network's computational mechanisms for generating neural responses the same as those in the brain? Without a systematic approach to extracting and understanding computational mechanisms from deep neural network models, it can be difficult both to assess the degree of utility of deep learning approaches in neuroscience, and to extract experimentally testable hypotheses from deep networks. We develop such a systematic approach by combining dimensionality reduction and modern attribution methods for determining the relative importance of interneurons for specific visual computations. We apply this approach to deep network models of the retina, revealing a conceptual understanding of how the retina acts as a predictive feature extractor that signals deviations from expectations for diverse spatiotemporal stimuli. For each stimulus, our extracted computational mechanisms are consistent with prior scientific literature, and in one case yields a new mechanistic hypothesis. Thus overall, this work not only yields insights into the computational mechanisms underlying the striking predictive capabilities of the retina, but also places the framework of deep networks as neuroscientific models on firmer theoretical foundations, by providing a new roadmap to go beyond comparing neural representations to extracting and understand computational mechanisms.

Visual information arriving at the retina is transmitted to the brain by signals in the optic nerve, and the brain must rely solely on these signals to make inferences about the visual world. Previous work has probed the content of these signals by directly reconstructing images from retinal activity using linear regression or nonlinear regression with neural networks. Maximum a posteriori (MAP) reconstruction using retinal encoding models and separately-trained natural image priors offers a more general and principled approach. We develop a novel method for approximate MAP reconstruction that combines a generalized linear model for retinal responses to light, including their dependence on spike history and spikes of neighboring cells, with the image prior implicitly embedded in a deep convolutional neural network trained for image denoising. We use this method to reconstruct natural images from ex vivo simultaneously-recorded spikes of hundreds of retinal ganglion cells uniformly sampling a region of the retina. The method produces reconstructions that match or exceed the state-of-the-art in perceptual similarity and exhibit additional fine detail, while using substantially fewer model parameters than previous approaches. The use of more rudimentary encoding models (a linear-nonlinear-Poisson cascade) or image priors (a 1/f spectral model) significantly reduces reconstruction performance, indicating the essential role of both components in achieving high-quality reconstructed images from the retinal signal.

Visual processing in the retina has been studied in great detail at all levels such that a comprehensive picture of the retina's cell types and the many neural circuits they form is emerging. However, the currently best performing models of retinal function are black-box CNN models which are agnostic to such biological knowledge.

In the early visual system, high dimensional natural stimuli are encoded into the trains of neuronal spikes that transmit the information to the brain to produce perception. However, is all the visual scene information required to explain the neuronal responses? In this work, we search for answers to this question by developing a joint model of the natural visual input and neuronal responses using the Information Bottleneck (IB) framework that can represent features of the input data into a few latent variables that play a role in the prediction of the outputs. The correlations between data samples acquired from published experiments on ex-vivo retinas are accounted for in the model by a Gaussian Process (GP) prior. The proposed IB-GP model performs competitively to the state-of-the-art feedforward convolutional networks in predicting spike responses to natural stimuli.

However, existing linear techniques for neural decoding may not fully reveal or exploit the fidelity of the neural signal.

Here we go beyond previous theories to analyze how a simple linear retinal encoding model with different convolutional cell types efficiently encodes naturalistic spatiotemporal movies given a fixed firing rate budget.

Recent advances in large-scale electrical and optical recording have made it possible to record and stimulate neural circuits at unprecedented scale and resolution [Jun et al., 2017, Kipke et al., 2008,

It is prohibitive to parameterize a natural movie and its respective retinal encoding fully.