The covariance perceptron: A new paradigm for classification and processing of time series in recurrent neuronal networks.

Learning in neuronal networks has developed in many directions, in particular to reproduce cognitive tasks like image recognition and speech processing. Implementations have been inspired by stereotypical neuronal responses like tuning curves in the visual system, where, for example, ON/OFF cells fire or not depending on the contrast in their receptive fields. Classical models of neuronal networks therefore map a set of input signals to a set of activity levels in the output of the network. Each category of inputs is thereby predominantly characterized by its mean. In the case of time series, fluctuations around this mean constitute noise in this view. For this paradigm, the high variability exhibited by the cortical activity may thus imply limitations or constraints, which have been discussed for many years. For example, the need for averaging neuronal activity over long periods or large groups of cells to assess a robust mean and to diminish the effect of noise correlations. To reconcile robust computations with variable neuronal activity, we here propose a conceptual change of perspective by employing variability of activity as the basis for stimulus-related information to be learned by neurons, rather than merely being the noise that corrupts the mean signal. In this new paradigm both afferent and recurrent weights in a network are tuned to shape the input-output mapping for covariances, the second-order statistics of the fluctuating activity. When including time lags, covariance patterns define a natural metric for time series that capture their propagating nature. We develop the theory for classification of time series based on their spatio-temporal covariances, which reflect dynamical properties. We demonstrate that recurrent connectivity is able to transform information contained in the temporal structure of the signal into spatial covariances. Finally, we use the MNIST database to show how the covariance perceptron can capture specific second-order statistical patterns generated by moving digits.

Model-based whole-brain effective connectivity to study distributed cognition in health and disease.

Neuroimaging techniques are now widely used to study human cognition. The functional associations between brain areas have become a standard proxy to describe how cognitive processes are distributed across the brain network. Among the many analysis tools available, dynamic models of brain activity have been developed to overcome the limitations of original connectivity measures such as functional connectivity. This goes in line with the many efforts devoted to the assessment of directional interactions between brain areas from the observed neuroimaging activity. This opinion article provides an overview of our model-based whole-brain effective connectivity to analyze fMRI data, while discussing the pros and cons of our approach with respect to other established approaches. Our framework relies on the multivariate Ornstein-Uhlenbeck (MOU) process and is thus referred to as MOU-EC. Once tuned, the model provides a directed connectivity estimate that reflects the dynamical state of BOLD activity, which can be used to explore cognition. We illustrate this approach using two applications on task-evoked fMRI data. First, as a connectivity measure, MOU-EC can be used to extract biomarkers for task-specific brain coordination, understood as the patterns of areas exchanging information. The multivariate nature of connectivity measures raises several challenges for whole-brain analysis, for which machine-learning tools present some advantages over statistical testing. Second, we show how to interpret changes in MOU-EC connections in a collective and model-based manner, bridging with network analysis. Our framework provides a comprehensive set of tools that open exciting perspectives to study distributed cognition, as well as neuropathologies.

Imaging Connectomics and the Understanding of Brain Diseases.

Neuroimaging-based personalized medicine is emerging to characterize brain disorders and their evolution at the patient level. In this chapter, we present the most classic methods used to infer large-scale brain connectivity based on functional MRI. We adopt a modeling perspective where every connectivity measure is linked to a specific model that allows to interpret the connectivity estimate. This perspective allows to analyze the quality of retrieved connectivity profiles in terms of modeling error and estimation error. In the first part of the chapter, we present undirected functional connectivity (Pearson's correlation and MI) and effective connectivity (partial correlation), as well as directed effective connectivity (VAR, MOU, Granger causality, DCM). In addition, some of these measures correspond to fully connected graphs (Pearson's correlation) while others to sparse ones (MOU, DCM), where the sparsity can come from the integration of functional and structural data. In the second part, we claim that machine learning tools are better suited than null-hypothesis testing to link the estimated connectomes with diagnosis and prognosis of neuropsychiatric diseases. Finally, we propose that linear models and features selection are preferable to more complex and nonlinear tools (when prediction performance is on a par) for building interpretable algorithms to predict clinical variables.

Extracting orthogonal subject- and condition-specific signatures from fMRI data using whole-brain effective connectivity.

The study of brain communication based on fMRI data is often limited because such measurements are a mixture of session-to-session variability with subject- and condition-related information. Disentangling these contributions is crucial for real-life applications, in particular when only a few recording sessions are available. The present study aims to define a reliable standard for the extraction of multiple signatures from fMRI data, while verifying that they do not mix information about the different modalities (e.g., subjects and conditions such as tasks performed by them). In particular, condition-specific signatures should not be contaminated by subject-related information, since they aim to generalize over subjects. Practically, signatures correspond to subnetworks of directed interactions between brain regions (typically 100 covering the whole brain) supporting the subject and condition identification for single fMRI sessions. The key for robust prediction is using effective connectivity instead of functional connectivity. Our method demonstrates excellent generalization capabilities for subject identification in two datasets, using only a few sessions per subject as reference. Using another dataset with resting state and movie viewing, we show that the two signatures related to subjects and tasks correspond to distinct subnetworks, which are thus topologically orthogonal. Our results set solid foundations for applications tailored to individual subjects, such as clinical diagnostic.

Multiple Choice Neurodynamical Model of the Uncertain Option Task.

The uncertain option task has been recently adopted to investigate the neural systems underlying the decision confidence. Latterly single neurons activity has been recorded in lateral intraparietal cortex of monkeys performing an uncertain option task, where the subject is allowed to opt for a small but sure reward instead of making a risky perceptual decision. We propose a multiple choice model implemented in a discrete attractors network. This model is able to reproduce both behavioral and neurophysiological experimental data and therefore provides support to the numerous perspectives that interpret the uncertain option task as a sensory-motor association. The model explains the behavioral and neural data recorded in monkeys as the result of the multistable attractor landscape and produces several testable predictions. One of these predictions may help distinguish our model from a recently proposed continuous attractor model.

Neural correlates of metacognition: A critical perspective on current tasks.

Humans have a remarkable ability to reflect upon their behavior and mental processes, a capacity known as metacognition. Recent neurophysiological experiments have attempted to elucidate the neural correlates of metacognition in other species. Despite this increased attention, there is still no operational definition of metacognition and the ability of behavioral tasks to reflect metacognition is the subject of debate. The most widely used task for studying metacognition in animals, the uncertain-option task, has been criticized because it can be solved by simple associative mechanisms. Here we propose a broad perspective that generalizes those critiques to another task, post-decision wagering. Moreover, we extend this critical view to account for recent neurophysiological evidence. We argue these tasks are simple enough that any animal could solve them using very simple mechanisms such as sensory-motor associations. In this case, it is impossible to know whether all animals are metacognitive, or if the tasks are simply not appropriate. Therefore, we suggest using better defined concepts until a suitable task for metacognition is available.

Confidence through consensus: a neural mechanism for uncertainty monitoring.

Models that integrate sensory evidence to a threshold can explain task accuracy, response times and confidence, yet it is still unclear how confidence is encoded in the brain. Classic models assume that confidence is encoded in some form of balance between the evidence integrated in favor and against the selected option. However, recent experiments that measure the sensory evidence's influence on choice and confidence contradict these classic models. We propose that the decision is taken by many loosely coupled modules each of which represent a stochastic sample of the sensory evidence integral. Confidence is then encoded in the dispersion between modules. We show that our proposal can account for the well established relations between confidence, and stimuli discriminability and reaction times, as well as the fluctuations influence on choice and confidence.

The Encoding of Decision Difficulty and Movement Time in the Primate Premotor Cortex.

Estimating the difficulty of a decision is a fundamental process to elaborate complex and adaptive behaviour. In this paper, we show that the movement time of behaving monkeys performing a decision-making task is correlated with decision difficulty and that the activity of a population of neurons in ventral Premotor cortex correlates with the movement time. Moreover, we found another population of neurons that encodes the discriminability of the stimulus, thereby supplying another source of information about the difficulty of the decision. The activity of neurons encoding the difficulty can be produced by very different computations. Therefore, we show that decision difficulty can be encoded through three different mechanisms: 1. Switch time coding, 2. rate coding and 3. binary coding. This rich representation reflects the basis of different functional aspects of difficulty in the making of a decision and the possible role of difficulty estimation in complex decision scenarios.

The influence of spatiotemporal structure of noisy stimuli in decision making.

Decision making is a process of utmost importance in our daily lives, the study of which has been receiving notable attention for decades. Nevertheless, the neural mechanisms underlying decision making are still not fully understood. Computational modeling has revealed itself as a valuable asset to address some of the fundamental questions. Biophysically plausible models, in particular, are useful in bridging the different levels of description that experimental studies provide, from the neural spiking activity recorded at the cellular level to the performance reported at the behavioral level. In this article, we have reviewed some of the recent progress made in the understanding of the neural mechanisms that underlie decision making. We have performed a critical evaluation of the available results and address, from a computational perspective, aspects of both experimentation and modeling that so far have eluded comprehension. To guide the discussion, we have selected a central theme which revolves around the following question: how does the spatiotemporal structure of sensory stimuli affect the perceptual decision-making process? This question is a timely one as several issues that still remain unresolved stem from this central theme. These include: (i) the role of spatiotemporal input fluctuations in perceptual decision making, (ii) how to extend the current results and models derived from two-alternative choice studies to scenarios with multiple competing evidences, and (iii) to establish whether different types of spatiotemporal input fluctuations affect decision-making outcomes in distinctive ways. And although we have restricted our discussion mostly to visual decisions, our main conclusions are arguably generalizable; hence, their possible extension to other sensory modalities is one of the points in our discussion.

Confidence-related decision making.

Neurons have been recorded that reflect in their firing rates the confidence in a decision. Here we show how this could arise as an emergent property in an integrate-and-fire attractor network model of decision making. The attractor network has populations of neurons that respond to each of the possible choices, each biased by the evidence for that choice, and there is competition between the attractor states until one population wins the competition and finishes with high firing that represents the decision. Noise resulting from the random spiking times of individual neurons makes the decision making probabilistic. We also show that a second attractor network can make decisions based on the confidence in the first decision. This system is supported by and accounts for neuronal responses recorded during decision making and makes predictions about the neuronal activity that will be found when a decision is made about whether to stay with a first decision or to abort the trial and start again. The research shows how monitoring can be performed in the brain and this has many implications for understanding cognitive functioning.