Sensory processing arises from the communication between neural populations across multiple brain areas. While the widespread presence of neural response variability shared throughout a neural population limits the amount of stimulus-related information those populations can accurately represent, how this variability affects the interareal communication of sensory information is unknown. We propose a mathematical framework to understand the impact of neural population response variability on sensory information transmission. We combine linear Fisher information, a metric connecting stimulus representation and variability, with the framework of communication subspaces, which suggests that functional mappings between cortical populations are low-dimensional relative to the space of population activity patterns. From this, we partition Fisher information depending on the alignment between the population covariance and the mean tuning direction projected onto the communication subspace or its orthogonal complement. We provide mathematical and numerical analyses of our proposed decomposition of Fisher information and examine theoretical scenarios that demonstrate how to leverage communication subspaces for flexible routing and gating of stimulus information. This work will provide researchers investigating interareal communication with a theoretical lens through which to understand sensory information transmission and guide experimental design.

Computational neuroscience studies have shown that the structure of neural variability to an unchanged stimulus affects the amount of information encoded. Some artificial deep neural networks, such as those with Monte Carlo dropout layers, also have variable responses when the input is fixed. However, the structure of the trial-by-trial neural covariance in neural networks with dropout has not been studied, and its role in decoding accuracy is unknown. We studied the above questions in a convolutional neural network model with dropout in both the training and testing phases. We found that trial-by-trial correlation between neurons (i.e., noise correlation) is positive and low dimensional. Neurons that are close in a feature map have larger noise correlation. These properties are surprisingly similar to the findings in the visual cortex. We further analyzed the alignment of the main axes of the covariance matrix. We found that different images share a common trial-by-trial noise covariance subspace, and they are aligned with the global signal covariance. This evidence that the noise covariance is aligned with signal covariance suggests that noise covariance in dropout neural networks reduces network accuracy, which we further verified directly with a trial-shuffling procedure commonly used in neuroscience. These findings highlight a previously overlooked aspect of dropout layers that can affect network performance. Such dropout networks could also potentially be a computational model of neural variability.

Segmenting visual stimuli into distinct groups of features and visual objects is central to visual function. Classical psychophysical methods have helped uncover many rules of human perceptual segmentation, and recent progress in machine learning has produced successful algorithms. Yet, the computational logic of human segmentation remains unclear, partially because we lack well-controlled paradigms to measure perceptual segmentation maps and compare models quantitatively. Here we propose a new, integrated approach: given an image, we measure multiple pixel-based same-different judgments and perform model-based reconstruction of the underlying segmentation map. The reconstruction is robust to several experimental manipulations and captures the variability of individual participants. We demonstrate the validity of the approach on human segmentation of natural images and composite textures. We show that image uncertainty affects measured human variability, and it influences how participants weigh different visual features. Because any putative segmentation algorithm can be inserted to perform the reconstruction, our paradigm affords quantitative tests of theories of perception as well as new benchmarks for segmentation algorithms.

Divisive normalization, a prominent descriptive model of neural activity, is employed by theories of neural coding across many different brain areas. Yet, the relationship between normalization and the statistics of neural responses beyond single neurons remains largely unexplored. Here we focus on noise correlations, a widely studied pairwise statistic, because its stimulus and state dependence plays a central role in neural coding. Existing models of covariability typically ignore normalization despite empirical evidence suggesting it affects correlation structure in neural populations. We therefore propose a pairwise stochastic divisive normalization model that accounts for the effects of normalization and other factors on covariability. We first show that normalization modulates noise correlations in qualitatively different ways depending on whether normalization is shared between neurons, and we discuss how to infer when normalization signals are shared. We then apply our model to calcium imaging data from mouse primary visual cortex (V1), and find that it accurately fits the data, often outperforming a popular alternative model of correlations. Our analysis indicates that normalization signals are often shared between V1 neurons in this dataset. Our model will enable quantifying the relation between normalization and covariability in a broad range of neural systems, which could provide new constraints on circuit mechanisms of normalization and their role in information transmission and representation.

We propose a family of probabilistic segmentation algorithms for videos that rely on a generative model capturing static and dynamic natural image statistics. Our framework adopts flexibly regularized mixture models (FlexMM) [1], an efficient method to combine mixture distributions across different data sources. FlexMMs of Student-t distributions successfully segment static natural images, through uncertainty-based information sharing between hidden layers of CNNs. We further extend this approach to videos and exploit FlexMM to propagate segment labels across space and time. We show that temporal propagation improves temporal consistency of segmentation, reproducing qualitatively a key aspect of human perceptual grouping. Besides, Student-t distributions can capture statistics of optical flows of natural movies, which represent apparent motion in the video. Integrating these motion cues in our temporal FlexMM further enhances the segmentation of each frame of natural movies. Our probabilistic dynamic segmentation algorithms thus provide a new framework to study uncertainty in human dynamic perceptual segmentation.

Skilled behavior often displays signatures of Bayesian inference. In order for the brain to implement the required computations, neuronal activity must carry accurate information about the uncertainty of sensory inputs. Two major approaches have been proposed to study neuronal representations of uncertainty. The first one, the Bayesian decoding approach, aims primarily at decoding the posterior probability distribution of the stimulus from population activity using Bayes' rule, and indirectly yields uncertainty estimates as a by-product. The second one, which we call the correlational approach, searches for specific features of neuronal activity (such as tuning-curve width and maximum firing-rate) which correlate with uncertainty. To compare these two approaches, we derived a new normative model of sound source localization by Interaural Time Difference (ITD), that reproduces a wealth of behavioral and neural observations. We found that several features of neuronal activity correlated with uncertainty on average, but none provided an accurate estimate of uncertainty on a trial-by-trial basis, indicating that the correlational approach may not reliably identify which aspects of neuronal responses represent uncertainty. In contrast, the Bayesian decoding approach reveals that the activity pattern of the entire population was required to reconstruct the trial-to-trial posterior distribution with Bayes' rule. These results suggest that uncertainty is unlikely to be represented in a single feature of neuronal activity, and highlight the importance of using a Bayesian decoding approach when exploring the neural basis of uncertainty.

Texture synthesis models are important tools for understanding visual processing. In particular, statistical approaches based on neurally relevant features have been instrumental in understanding aspects of visual perception and of neural coding. New deep learning-based approaches further improve the quality of synthetic textures. Yet, it is still unclear why deep texture synthesis performs so well, and applications of this new framework to probe visual perception are scarce. Here, we show that distributions of deep convolutional neural network (CNN) activations of a texture are well described by elliptical distributions and therefore, following optimal transport theory, constraining their mean and covariance is sufficient to generate new texture samples. Then, we propose the natural geodesics (ie the shortest path between two points) arising with the optimal transport metric to interpolate between arbitrary textures. Compared to other CNN-based approaches, our interpolation method appears to match more closely the geometry of texture perception, and our mathematical framework is better suited to study its statistical nature. We apply our method by measuring the perceptual scale associated to the interpolation parameter in human observers, and the neural sensitivity of different areas of visual cortex in macaque monkeys.

Neural responses are known to be variable. In order to understand how this neural variability constrains behavioral performance, we need to be able to measure the reliability with which a sensory stimulus is encoded in a given population. However, such measures are challenging for two reasons: First, they must take into account noise correlations which can have a large influence on reliability. Second, they need to be as efficient as possible, since the number of trials available in a set of neural recording is usually limited by experimental constraints. Traditionally, cross-validated decoding has been used as a reliability measure, but it only provides a lower bound on reliability and underestimates reliability substantially in small datasets. We show that, if the number of trials per condition is larger than the number of neurons, there is an alternative, direct estimate of reliability which consistently leads to smaller errors and is much faster to compute. The superior performance of the direct estimator is evident both for simulated data and for neuronal population recordings from macaque primary visual cortex. Furthermore we propose generalizations of the direct estimator which measure changes in stimulus encoding across conditions and the impact of correlations on encoding and decoding, typically denoted by Ishuffle and Idiag respectively.

Spatial context in images induces perceptual phenomena associated with salience and modulates the responses of neurons in primary visual cortex (V1). However, the computational and ecological principles underlying contextual effects are incompletely understood. We introduce a model of natural images that includes grouping and segmentation of neighboring features based on their joint statistics, and we interpret the firing rates of V1 neurons as performing optimal recognition in this model. We show that this leads to a substantial generalization of divisive normalization, a computation that is ubiquitous in many neural areas and systems. A main novelty in our model is that the influence of the context on a target stimulus is determined by their degree of statistical dependence. We optimized the parameters of the model on natural image patches, and then simulated neural and perceptual responses on stimuli used in classical experiments. The model reproduces some rich and complex response patterns observed in V1, such as the contrast dependence, orientation tuning and spatial asymmetry of surround suppression, while also allowing for surround facilitation under conditions of weak stimulation. It also mimics the perceptual salience produced by simple displays, and leads to readily testable predictions. Our results provide a principled account of orientation-based contextual modulation in early vision and its sensitivity to the homogeneity and spatial arrangement of inputs, and lends statistical support to the theory that V1 computes visual salience.

A central hypothesis about early visual processing is that it represents inputs in a coordinate system matched to the statistics of natural scenes. Simple versions of this lead to Gabor-like receptive fields and divisive gain modulation from local surrounds; these have led to influential neural and psychological models of visual processing. However, these accounts are based on an incomplete view of the visual context surrounding each point. Here, we consider an approximate model of linear and non-linear correlations between the responses of spatially distributed Gabor-like receptive fields, which, when trained on an ensemble of natural scenes, unifies a range of spatial context effects. The full model accounts for neural surround data in primary visual cortex (V1), provides a statistical foundation for perceptual phenomena associated with Lis (2002) hypothesis that V1 builds a saliency map, and fits data on the tilt illusion.

In this paper we consider the problem of sensorimotor coordination in a Bayesian framework. To this end we introduce a novel kind of Dynamic Bayesian Network serving as the core tool to integrate active vision and task-constrained motor behaviors. The proposed system is put into work by addressing the challenging task of realistic drawing performed by a robotic agent, namely a 7-DOF anthropomorphic manipulator. Simulation results are compared to those obtained by eye-tracked human subjects involved in drawing experiments.

In this paper we address the challenging problem of sensorimotor integration, with reference to eye-hand coordination of an artificial agent engaged in a natural drawing task. Under the assumption that eye-hand coupling influences observed movements, a motor continuity hypothesis is exploited to account for how gaze shifts are constrained by hand movements. A Bayesian model of such coupling is presented in the form of a novel Dynamic Bayesian Network, namely an Input–Output Coupled Hidden Markov Model. Simulation results are compared to those obtained by eye-tracked human subjects involved in drawing experiments.