We release NSD-Imagery, a benchmark dataset of human fMRI activity paired with mental images, to complement the existing Natural Scenes Dataset (NSD), a large-scale dataset of fMRI activity paired with seen images that enabled unprecedented improvements in fMRI-to-image reconstruction efforts. Recent models trained on NSD have been evaluated only on seen image reconstruction. Using NSD-Imagery, it is possible to assess how well these models perform on mental image reconstruction. This is a challenging generalization requirement because mental images are encoded in human brain activity with relatively lower signal-to-noise and spatial resolution; however, generalization from seen to mental imagery is critical for real-world applications in medical domains and brain-computer interfaces, where the desired information is always internally generated. We provide benchmarks for a suite of recent NSD-trained open-source visual decoding models (MindEye1, MindEye2, Brain Diffuser, iCNN, Takagi et al.) on NSD-Imagery, and show that the performance of decoding methods on mental images is largely decoupled from performance on vision reconstruction. We further demonstrate that architectural choices significantly impact cross-decoding performance: models employing simple linear decoding architectures and multi-modal feature decoding generalize better to mental imagery, while complex architectures tend to overfit visual training data. Our findings indicate that mental imagery datasets are critical for the development of practical applications, and establish NSD-Imagery as a useful resource for better aligning visual decoding methods with this goal.

Measurements of neural responses to identically repeated experimental events often exhibit large amounts of variability. This noise is distinct from signal, operationally defined as the average expected response across repeated trials for each given event. Accurately distinguishing signal from noise is important, as each is a target that is worthy of study (many believe noise reflects important aspects of brain function) and it is important not to confuse one for the other. Here, we describe a principled modeling approach in which response measurements are explicitly modeled as the sum of samples from multivariate signal and noise distributions. In our proposed method-termed Generative Modeling of Signal and Noise (GSN)-the signal distribution is estimated by subtracting the estimated noise distribution from the estimated data distribution. Importantly, GSN improves estimates of the signal distribution, but does not provide improved estimates of responses to individual events. We validate GSN using ground-truth simulations and show that it compares favorably with related methods. We also demonstrate the application of GSN to empirical fMRI data to illustrate a simple consequence of GSN: by disentangling signal and noise components in neural responses, GSN denoises principal components analysis and improves estimates of dimensionality. We end by discussing other situations that may benefit from GSN's characterization of signal and noise, such as estimation of noise ceilings for computational models of neural activity. A code toolbox for GSN is provided with both MATLAB and Python implementations.

Brain activity patterns in high-level visual cortex support accurate linear classification of visual concepts (e.g., objects or scenes). It has long been appreciated that the accuracy of linear classification in any brain area depends on the geometry of its concept manifolds-sets of brain activity patterns that encode images of a concept. However, it is unclear how the geometry of concept manifolds differs between regions of visual cortex that support accurate classification and those that don't, or how it differs between visual cortex and deep neural networks (DNNs). We estimated geometric properties of concept manifolds that, per a recent theory, directly determine the accuracy of simple "few-shot" linear classifiers. Using a large fMRI dataset, we show that variation in classification accuracy across human visual cortex is driven by a variation in a single geometric property: the distance between manifold centers ("geometric Signal"). In contrast, variation in classification accuracy across early and mid DNN layers is driven by an increase in the effective number of manifold dimensions ("Dimensionality"). Despite this difference in the geometric properties that affect few-shot classification performance in the brain and DNNs, we find that Signal and Dimensionality are strongly, negatively correlated: when Signal increases across brain regions or DNN layers, Dimensionality decreases, and vice versa. We conclude that early visual cortical areas and DNN layers deploy different geometric strategies for accurate linear classification of concepts, even though both are subject to the same constraint.

Previous studies in neurophysiology have shown that neurons exhibit trial-by-trial correlated activity and that such noise correlations (NCs) greatly impact the accuracy of population codes. Meanwhile, multivariate pattern analysis (MVPA) has become a mainstream approach in functional magnetic resonance imaging (fMRI), but it remains unclear how NCs between voxels influence MVPA performance. Here, we tackle this issue by combining voxel-encoding modeling and MVPA. We focus on a well-established form of NC, tuning-compatible noise correlation (TCNC), whose sign and magnitude are systematically related to the tuning similarity between two units. We show that this form of voxelwise NCs can improve MVPA performance if NCs are sufficiently strong. We also confirm these results using standard information-theoretic analyses in computational neuroscience. In the same theoretical framework, we further demonstrate that the effects of noise correlations at both the neuronal level and the voxel level may manifest differently in typical fMRI data, and their effects are modulated by tuning heterogeneity. Our results provide a theoretical foundation to understand the effect of correlated activity on population codes in macroscopic fMRI data. Our results also suggest that future fMRI research could benefit from a closer examination of the correlational structure of multivariate responses, which is not directly revealed by conventional MVPA approaches.

Visual neurons respond to static images with specific dynamics: neuronal responses sum sub-additively over time, reduce in amplitude with repeated or sustained stimuli (neuronal adaptation), and are slower at low stimulus contrast. Here, we propose a simple model that predicts these seemingly disparate response patterns observed in a diverse set of measurements-intracranial electrodes in patients, fMRI, and macaque single unit spiking. The model takes a time-varying contrast time course of a stimulus as input, and produces predicted neuronal dynamics as output. Model computation consists of linear filtering, expansive exponentiation, and a divisive gain control. The gain control signal relates to but is slower than the linear signal, and this delay is critical in giving rise to predictions matched to the observed dynamics. Our model is simpler than previously proposed related models, and fitting the model to intracranial EEG data uncovers two regularities across human visual field maps: estimated linear filters (temporal receptive fields) systematically differ across and within visual field maps, and later areas exhibit more rapid and substantial gain control. The model is further generalizable to account for dynamics of contrast-dependent spike rates in macaque V1, and amplitudes of fMRI BOLD in human V1.

Visual neuroscientists have discovered fundamental properties of neural representation through careful analysis of responses to controlled stimuli. Typically, different properties are studied and modeled separately. To integrate our knowledge, it is necessary to build general models that begin with an input image and predict responses to a wide range of stimuli. In this study, we develop a model that accepts an arbitrary band-pass grayscale image as input and predicts blood oxygenation level dependent (BOLD) responses in early visual cortex as output. The model has a cascade architecture, consisting of two stages of linear and nonlinear operations. The first stage involves well-established computations-local oriented filters and divisive normalization-whereas the second stage involves novel computations-compressive spatial summation (a form of normalization) and a variance-like nonlinearity that generates selectivity for second-order contrast. The parameters of the model, which are estimated from BOLD data, vary systematically across visual field maps: compared to primary visual cortex, extrastriate maps generally have larger receptive field size, stronger levels of normalization, and increased selectivity for second-order contrast. Our results provide insight into how stimuli are encoded and transformed in successive stages of visual processing.

We propose a novel hierarchical, nonlinear model that predicts brain activity in area V1 evoked by natural images. In the study reported here brain activity was measured by means of functional magnetic resonance imaging (fMRI), a noninvasive technique that provides an indirect measure of neural activity pooled over a small volume (~ 2mm cube) of brain tissue. Our model, which we call the SpAM V1 model, is based on the reasonable assumption that fMRI measurements reflect the (possibly nonlinearly) pooled, rectified output of a large population of simple and complex cells in V1. It has a hierarchical filtering stage that consists of three layers: model simple cells, model complex cells, and a third layer in which the complex cells are linearly pooled (called “pooled-complex” cells). The pooling stage then obtains the measured fMRI signals as a sparse additive model (SpAM) in which a sparse nonparametric (nonlinear) combination of model complex cell and model pooled-complex cell outputs are summed. Our results show that the SpAM V1 model predicts fMRI responses evoked by natural images better than a benchmark model that only provides linear pooling of model complex cells. Furthermore, the spatial receptive fields, frequency tuning and orientation tuning curves of the SpAM V1 model estimated for each voxel appears to be consistent with the known properties of V1, and with previous analyses of this data set. A visualization procedure applied to the SpAM V1 model shows that most of the nonlinear pooling consists of simple compressive or saturating nonlinearities.