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Neural population responses in sensory systems are driven by external physical stimuli. This stimulus-response relationship is typically characterized by receptive fields, which have been estimated by neural system identification approaches. Such models usually require a large amount of training data, yet, the recording time for animal experiments is limited, giving rise to epistemic uncertainty for the learned neural transfer functions. While deep neural network models have demonstrated excellent power on neural prediction, they usually do not provide the uncertainty of the resulting neural representations and derived statistics, such as most exciting inputs (MEIs), from in silico experiments. Here, we present a Bayesian system identification approach to predict neural responses to visual stimuli, and explore whether explicitly modeling network weight variability can be beneficial for identifying neural response properties. To this end, we use variational inference to estimate the posterior distribution of each model weight given the training data. Tests with different neural datasets demonstrate that this method can achieve higher or comparable performance on neural prediction, with a much higher data efficiency compared to Monte Carlo dropout methods and traditional models using point estimates of the model parameters. At the same time, our variational method provides us with an effectively infinite ensemble, avoiding the idiosyncrasy of any single model, to generate MEIs. It allows to estimate the uncertainty of stimulus-response function, which we have found to be negatively correlated with the predictive performance at model level and may serve to evaluate models. Furthermore, our approach enables us to identify response properties with credible intervals and to determine whether the inferred features are meaningful by performing statistical tests on MEIs. Finally, in silico experiments show that our model generates stimuli driving neuronal activity significantly better than traditional models in the limited-data regime. Author summary: Neural system identification methods learn stimulus-response functions using experimental data to predict responses. These neuronal prediction models demand large amounts of training data, however, the recording time for each experiment is restricted, introducing the uncertainty about the neural features derived from trained models. Here, we present a Bayesian approach incorporating weight uncertainty to identify response functions and show that our method has higher or comparable predictive performance with a higher data efficiency compared to traditional methods using point estimates of model parameters. Additionally, our model provides an effective infinite ensemble to derive neural features, which avoid the idiosyncrasy of a single model. In this way, our method also allows us to estimate the uncertainty of the derived features and to conduct statistical tests on them. Generally, our Bayesian approach enables us to generate many similar stimuli to investigate biological information processing. [ABSTRACT FROM AUTHOR]

The retina transforms patterns of light into visual feature representations supporting behaviour. These representations are distributed across various types of retinal ganglion cells (RGCs), whose spatial and temporal tuning properties have been studied extensively in many model organisms, including the mouse. However, it has been difficult to link the potentially nonlinear retinal transformations of natural visual inputs to specific ethological purposes. Here, we discover a nonlinear selectivity to chromatic contrast in an RGC type that allows the detection of changes in visual context. We trained a convolutional neural network (CNN) model on large-scale functional recordings of RGC responses to natural mouse movies, and then used this model to search in silico for stimuli that maximally excite distinct types of RGCs. This procedure predicted centre colour opponency in transient suppressed-by-contrast (tSbC) RGCs, a cell type whose function is being debated. We confirmed experimentally that these cells indeed responded very selectively to Green-OFF, UV-ON contrasts. This type of chromatic contrast was characteristic of transitions from ground to sky in the visual scene, as might be elicited by head or eye movements across the horizon. Because tSbC cells performed best among all RGC types at reliably detecting these transitions, we suggest a role for this RGC type in providing contextual information (i.e. sky or ground) necessary for the selection of appropriate behavioural responses to other stimuli, such as looming objects. Our work showcases how a combination of experiments with natural stimuli and computational modelling allows discovering novel types of stimulus selectivity and identifying their potential ethological relevance., Competing Interests: LH, KS, CB, YD, YQ, DK, ZJ, GS, MB, PB, KF, AE, TE No competing interests declared, (© 2024, Höfling et al.)

Understanding how biological visual systems process information is challenging because of the nonlinear relationship between visual input and neuronal responses. Artificial neural networks allow computational neuroscientists to create predictive models that connect biological and machine vision. Machine learning has benefited tremendously from benchmarks that compare different model on the same task under standardized conditions. However, there was no standardized benchmark to identify state-of-the-art dynamic models of the mouse visual system. To address this gap, we established the SENSORIUM 2023 Benchmark Competition with dynamic input, featuring a new large-scale dataset from the primary visual cortex of ten mice. This dataset includes responses from 78,853 neurons to 2 hours of dynamic stimuli per neuron, together with the behavioral measurements such as running speed, pupil dilation, and eye movements. The competition ranked models in two tracks based on predictive performance for neuronal responses on a held-out test set: one focusing on predicting in-domain natural stimuli and another on out-of-distribution (OOD) stimuli to assess model generalization. As part of the NeurIPS 2023 competition track, we received more than 160 model submissions from 22 teams. Several new architectures for predictive models were proposed, and the winning teams improved the previous state-of-the-art model by 50%. Access to the dataset as well as the benchmarking infrastructure will remain online at www.sensorium-competition.net.

Understanding how biological visual systems process information is challenging due to the complex nonlinear relationship between neuronal responses and high-dimensional visual input. Artificial neural networks have already improved our understanding of this system by allowing computational neuroscientists to create predictive models and bridge biological and machine vision. During the Sensorium 2022 competition, we introduced benchmarks for vision models with static input (i.e. images). However, animals operate and excel in dynamic environments, making it crucial to study and understand how the brain functions under these conditions. Moreover, many biological theories, such as predictive coding, suggest that previous input is crucial for current input processing. Currently, there is no standardized benchmark to identify state-of-the-art dynamic models of the mouse visual system. To address this gap, we propose the Sensorium 2023 Benchmark Competition with dynamic input (https://www.sensorium-competition.net/). This competition includes the collection of a new large-scale dataset from the primary visual cortex of ten mice, containing responses from over 78,000 neurons to over 2 hours of dynamic stimuli per neuron. Participants in the main benchmark track will compete to identify the best predictive models of neuronal responses for dynamic input (i.e. video). We will also host a bonus track in which submission performance will be evaluated on out-of-domain input, using withheld neuronal responses to dynamic input stimuli whose statistics differ from the training set. Both tracks will offer behavioral data along with video stimuli. As before, we will provide code, tutorials, and strong pre-trained baseline models to encourage participation. We hope this competition will continue to strengthen the accompanying Sensorium benchmarks collection as a standard tool to measure progress in large-scale neural system identification models of the entire mouse visual hierarchy and beyond.