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Here we test our conceptual understanding of V1 function by asking two experimental questions: 1) How do neurons respond to the spatiotemporal structure contained in dynamic, natural scenes? and 2) What is the true range of visual responsiveness and predictability of neural responses obtained in an unbiased sample of neurons across all layers of cortex? We address these questions by recording responses to natural movie stimuli with 32 channel silicon probes. By simultaneously recording from cells in all layers, and taking all recorded cells, we reduce recording bias that results from hunting for neural responses evoked from drifting bars and gratings. A nonparametric model reveals that many cells that are visually responsive do not appear to be captured by standard receptive field models. Using nonlinear Radial Basis Function kernels in a support vector machine, we can explain the responses of some of these cells better than standard linear and phase-invariant complex cell models. This suggests that V1 neurons exhibit more complex and diverse responses than standard models can capture, ranging from simple and complex cells strongly driven by their classical receptive fields, to cells with more nonlinear receptive fields inferred from the nonparametric and RFB model, and cells that are not visually responsive despite robust firing.
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Orientation selectivity is the most striking feature of simple cell coding in V1 which has been shown to emerge from the reduction of higher-order correlations in natural images in a large variety of statistical image models. The most parsimonious one among these models is linear Independent Component Analysis (ICA), whereas second-order decorrelation transformations such as Principal Component Analysis (PCA) do not yield oriented filters. Because of this finding it has been suggested that the emergence of orientation selectivity may be explained by higher-order redundancy reduction. In order to assess the tenability of this hypothesis, it is an important empirical question how much more redundancies can be removed with ICA in comparison to PCA, or other second-order decorrelation methods. This question has not yet been settled, as over the last ten years contradicting results have been reported ranging from less than five to more than hundred percent extra gain for ICA. Here, we aim at resolving this conflict by presenting a very careful and comprehensive analysis using three evaluation criteria related to redundancy reduction: In addition to the multi-information and the average log-loss we compute, for the first time, complete rate-distortion curves for ICA in comparison with PCA. Without exception, we find that the advantage of the ICA filters is surprisingly small. Furthermore, we show that a simple spherically symmetric distribution with only two parameters can fit the data even better than the probabilistic model underlying ICA. Since spherically symmetric models are agnostic with respect to the specific filter shapes, we conlude that orientation selectivity is unlikely to play a critical role for redundancy reduction.
Response variability, as measured by fluctuating responses upon repeated performance of trials, is a major component of neural responses, and its characterization is key to interpret high dimensional population recordings. Response variability and covariability display predictable changes upon changes in stimulus and cognitive or behavioral state, providing an opportunity to test the predictive power of models of neural variability. Still, there is little agreement on which model to use as a building block for population-level analyses, and models of variability are often treated as a subject of choice. We investigate two competing models, the Doubly Stochastic Poisson (DSP) model assuming stochasticity at spike generation, and the Rectified Gaussian (RG) model that traces variability back to membrane potential variance, to analyze stimulus-dependent modulation of response statistics. Using a model of a pair of neurons, we demonstrate that the two models predict similar single-cell statistics. However, DSP and RG models have contradicting predictions on the joint statistics of spiking responses. In order to test the models against data, we build a population model to simulate stimulus change-related modulations in response statistics. We use unit recordings from the primary visual cortex of monkeys to show that while model predictions for variance are qualitatively similar to experimental data, only the RG models predictions are compatible with joint statistics. These results suggest that models using Poisson-like variability might fail to capture important properties of response statistics. We argue that membrane potential-level modelling of stochasticity provides an efficient strategy to model correlations.
It has been hypothesized that neural activities in the primary visual cortex (V1) represent a saliency map of the visual field to exogenously guide attention. This hypothesis has so far provided only qualitative predictions and their confirmations. We report this hypothesis first quantitative prediction, derived without free parameters, and its confirmation by human behavioral data. The hypothesis provides a direct link between V1 neural responses to a visual location and the saliency of that location to guide attention exogenously. In a visual input containing many bars, one of them saliently different from all the other bars which are identical to each other, saliency at the singletons location can be measured by the shortness of the reaction time in a visual search task to find the singleton. The hypothesis predicts quantitatively the whole distribution of the reaction times to find a singleton unique in color, orientation, and motion direction from the reaction times to find other types of singletons. The predicted distribution matches the experimentally observed distribution in all six human observers. A requirement for this successful prediction is a data-motivated assumption that V1 lacks neurons tuned simultaneously to color, orientation, and motion direction of visual inputs. Since evidence suggests that extrastriate cortices do have such neurons, we discuss the possibility that the extrastriate cortices play no role in guiding exogenous attention so that they can be devoted to other functional roles like visual decoding or endogenous attention.
When presented with information of any type, from music to language to mathematics, the human mind subconsciously arranges it into a network. A network puts pieces of information like musical notes, syllables or mathematical concepts into context by linking them together. These networks help our minds organize information and anticipate what is coming. Here we present two questions about network building. 1) Can humans more easily learn some types of networks than others? 2) Do humans find some links between ideas more surprising than others? The answer to both questions is Yes, and we explain why. The findings provide much-needed insight into the ways that humans learn about the networked world around them. Moreover, the study paves the way for future efforts seeking to optimize how information is presented to accelerate human learning.
Astrocytes affect neural transmission by a tight control via glutamate transporters on glutamate concentrations in direct vicinity to the synaptic cleft and by extracellular glutamate. Their relevance for information representation has been supported by in-vivo studies in ferret and mouse primary visual cortex. In ferret blocking glutamate transport pharmacologically broadened tuning curves and enhanced the response at preferred orientation. In knock-out mice with reduced expression of glutamate transporters sharpened tuning was observed. It is however unclear how focal and ambient changes in glutamate concentration affect stimulus representation. Here we develop a computational framework, which allows the investigation of synaptic and extrasynaptic effects of glutamate uptake on orientation tuning in recurrently connected network models with pinwheel-domain (ferret) or salt-and-pepper (mouse) organization. This model proposed that glutamate uptake shapes information representation when it affects the contribution of excitatory and inhibitory neurons to the network activity. Namely, strengthening the contribution of excitatory neurons generally broadens tuning and elevates the response. In contrast, strengthening the contribution of inhibitory neurons can have a sharpening effect on tuning. In addition local representational topology also plays a role: In the pinwheel-domain model effects were strongest within domains - regions where neighboring neurons share preferred orientations. Around pinwheels but also within salt-and-pepper networks the effects were less strong. Our model proposes that the pharmacological intervention in ferret increases the contribution of excitatory cells, while the reduced expression in mouse increases the contribution of inhibitory cells to network activity.
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