Evaluating Representational Similarity Measures from the Lens of Functional Correspondence

Neuroscience and artificial intelligence (AI) both face the challenge of interpreting high-dimensional neural data, where the comparative analysis of such data is crucial for revealing shared mechanisms and differences between these complex systems. Despite the widespread use of representational comparisons and the abundance classes of comparison methods, a critical question remains: which metrics are most suitable for these comparisons? While some studies evaluate metrics based on their ability to differentiate models of different origins or constructions (e.g., various architectures), another approach is to assess how well they distinguish models that exhibit distinct behaviors. To investigate this, we examine the degree of alignment between various representational similarity measures and behavioral outcomes, employing group statistics and a comprehensive suite of behavioral metrics for comparison. In our evaluation of eight commonly used representational similarity metrics in the visual domain -- spanning alignment-based, Canonical Correlation Analysis (CCA)-based, inner product kernel-based, and nearest-neighbor methods -- we found that metrics like linear Centered Kernel Alignment (CKA) and Procrustes distance, which emphasize the overall geometric structure or shape of representations, excelled in differentiating trained from untrained models and aligning with behavioral measures, whereas metrics such as linear predictivity, commonly used in neuroscience, demonstrated only moderate alignment with behavior. These insights are crucial for selecting metrics that emphasize behaviorally meaningful comparisons in NeuroAI research.

Soft Matching Distance: A metric on neural representations that captures single-neuron tuning

Common measures of neural representational (dis)similarity are designed to be insensitive to rotations and reflections of the neural activation space. Motivated by the premise that the tuning of individual units may be important, there has been recent interest in developing stricter notions of representational (dis)similarity that require neurons to be individually matched across networks. When two networks have the same size (i.e. same number of neurons), a distance metric can be formulated by optimizing over neuron index permutations to maximize tuning curve alignment. However, it is not clear how to generalize this metric to measure distances between networks with different sizes. Here, we leverage a connection to optimal transport theory to derive a natural generalization based on "soft" permutations. The resulting metric is symmetric, satisfies the triangle inequality, and can be interpreted as a Wasserstein distance between two empirical distributions. Further, our proposed metric avoids counter-intuitive outcomes suffered by alternative approaches, and captures complementary geometric insights into neural representations that are entirely missed by rotation-invariant metrics.

NeuroGen: activation optimized image synthesis for discovery neuroscience

Functional MRI (fMRI) is a powerful technique that has allowed us to characterize visual cortex responses to stimuli, yet such experiments are by nature constructed based on a priori hypotheses, limited to the set of images presented to the individual while they are in the scanner, are subject to noise in the observed brain responses, and may vary widely across individuals. In this work, we propose a novel computational strategy, which we call NeuroGen, to overcome these limitations and develop a powerful tool for human vision neuroscience discovery. NeuroGen combines an fMRI-trained neural encoding model of human vision with a deep generative network to synthesize images predicted to achieve a target pattern of macro-scale brain activation. We demonstrate that the reduction of noise that the encoding model provides, coupled with the generative network's ability to produce images of high fidelity, results in a robust discovery architecture for visual neuroscience. By using only a small number of synthetic images created by NeuroGen, we demonstrate that we can detect and amplify differences in regional and individual human brain response patterns to visual stimuli. We then verify that these discoveries are reflected in the several thousand observed image responses measured with fMRI. We further demonstrate that NeuroGen can create synthetic images predicted to achieve regional response patterns not achievable by the best-matching natural images. The NeuroGen framework extends the utility of brain encoding models and opens up a new avenue for exploring, and possibly precisely controlling, the human visual system.

Neural encoding with visual attention

Visual perception is critically influenced by the focus of attention. Due to limited resources, it is well known that neural representations are biased in favor of attended locations. Using concurrent eye-tracking and functional Magnetic Resonance Imaging (fMRI) recordings from a large cohort of human subjects watching movies, we first demonstrate that leveraging gaze information, in the form of attentional masking, can significantly improve brain response prediction accuracy in a neural encoding model. Next, we propose a novel approach to neural encoding by including a trainable soft-attention module. Using our new approach, we demonstrate that it is possible to learn visual attention policies by end-to-end learning merely on fMRI response data, and without relying on any eye-tracking. Interestingly, we find that attention locations estimated by the model on independent data agree well with the corresponding eye fixation patterns, despite no explicit supervision to do so. Together, these findings suggest that attention modules can be instrumental in neural encoding models of visual stimuli.

From Connectomic to Task-evoked Fingerprints: Individualized Prediction of Task Contrasts from Resting-state Functional Connectivity

Resting-state functional MRI (rsfMRI) yields functional connectomes that can serve as cognitive fingerprints of individuals. Connectomic fingerprints have proven useful in many machine learning tasks, such as predicting subject-specific behavioral traits or task-evoked activity. In this work, we propose a surface-based convolutional neural network (BrainSurfCNN) model to predict individual task contrasts from their resting-state fingerprints. We introduce a reconstructive-contrastive loss that enforces subject-specificity of model outputs while minimizing predictive error. The proposed approach significantly improves the accuracy of predicted contrasts over a well-established baseline. Furthermore, BrainSurfCNN's prediction also surpasses test-retest benchmark in a subject identification task.

A shared neural encoding model for the prediction of subject-specific fMRI response

The increasing popularity of naturalistic paradigms in fMRI (such as movie watching) demands novel strategies for multi-subject data analysis, such as use of neural encoding models. In the present study, we propose a shared convolutional neural encoding method that accounts for individual-level differences. Our method leverages multi-subject data to improve the prediction of subject-specific responses evoked by visual or auditory stimuli. We showcase our approach on high-resolution 7T fMRI data from the Human Connectome Project movie-watching protocol and demonstrate significant improvement over single-subject encoding models. We further demonstrate the ability of the shared encoding model to successfully capture meaningful individual differences in response to traditional task-based facial and scenes stimuli. Taken together, our findings suggest that inter-subject knowledge transfer can be beneficial to subject-specific predictive models.

Detecting abnormalities in resting-state dynamics: An unsupervised learning approach

Resting-state functional MRI (rs-fMRI) is a rich imaging modality that captures spontaneous brain activity patterns, revealing clues about the connectomic organization of the human brain. While many rs-fMRI studies have focused on static measures of functional connectivity, there has been a recent surge in examining the temporal patterns in these data. In this paper, we explore two strategies for capturing the normal variability in resting-state activity across a healthy population: (a) an autoencoder approach on the rs-fMRI sequence, and (b) a next frame prediction strategy. We show that both approaches can learn useful representations of rs-fMRI data and demonstrate their novel application for abnormality detection in the context of discriminating autism patients from healthy controls.

Machine learning in resting-state fMRI analysis

Machine learning techniques have gained prominence for the analysis of resting-state functional Magnetic Resonance Imaging (rs-fMRI) data. Here, we present an overview of various unsupervised and supervised machine learning applications to rs-fMRI. We present a methodical taxonomy of machine learning methods in resting-state fMRI. We identify three major divisions of unsupervised learning methods with regard to their applications to rs-fMRI, based on whether they discover principal modes of variation across space, time or population. Next, we survey the algorithms and rs-fMRI feature representations that have driven the success of supervised subject-level predictions. The goal is to provide a high-level overview of the burgeoning field of rs-fMRI from the perspective of machine learning applications.

Ensemble learning with 3D convolutional neural networks for connectome-based prediction

The specificty and sensitivity of resting state functional MRI (rs-fMRI) measurements depend on pre-processing choices, such as the parcellation scheme used to define regions of interest (ROIs). In this study, we critically evaluate the effect of brain parcellations on machine learning models applied to rs-fMRI data. Our experiments reveal a remarkable trend: On average, models with stochastic parcellations consistently perform as well as models with widely used atlases at the same spatial scale. We thus propose an ensemble learning strategy to combine the predictions from models trained on connectivity data extracted using different (e.g., stochastic) parcellations. We further present an implementation of our ensemble learning strategy with a novel 3D Convolutional Neural Network (CNN) approach. The proposed CNN approach takes advantage of the full-resolution 3D spatial structure of rs-fMRI data and fits non-linear predictive models. Our ensemble CNN framework overcomes the limitations of traditional machine learning models for connectomes that often rely on region-based summary statistics and/or linear models. We showcase our approach on a classification (autism patients versus healthy controls) and a regression problem (prediction of subject's age), and report promising results.

3D Convolutional Neural Networks for Classification of Functional Connectomes

Resting-state functional MRI (rs-fMRI) scans hold the potential to serve as a diagnostic or prognostic tool for a wide variety of conditions, such as autism, Alzheimer's disease, and stroke. While a growing number of studies have demonstrated the promise of machine learning algorithms for rs-fMRI based clinical or behavioral prediction, most prior models have been limited in their capacity to exploit the richness of the data. For example, classification techniques applied to rs-fMRI often rely on region-based summary statistics and/or linear models. In this work, we propose a novel volumetric Convolutional Neural Network (CNN) framework that takes advantage of the full-resolution 3D spatial structure of rs-fMRI data and fits non-linear predictive models. We showcase our approach on a challenging large-scale dataset (ABIDE, with N > 2,000) and report state-of-the-art accuracy results on rs-fMRI-based discrimination of autism patients and healthy controls.