Correlations of noise in neural population activity are thought to limit the amount of information contained in such population activity, whereas decorrelation is suggested to increase information content. Here the authors show that decorrelation does not imply an increase in information, and only certain types of correlations limit information content. Computational strategies used by the brain strongly depend on the amount of information that can be stored in population activity, which in turn strongly depends on the pattern of noise correlations. In vivo, noise correlations tend to be positive and proportional to the similarity in tuning properties. Such correlations are thought to limit information, which has led to the suggestion that decorrelation increases information. In contrast, we found, analytically and numerically, that decorrelation does not imply an increase in information. Instead, the only information-limiting correlations are what we refer to as differential correlations: correlations proportional to the product of the derivatives of the tuning curves. Unfortunately, differential correlations are likely to be very small and buried under correlations that do not limit information, making them particularly difficult to detect. We found, however, that the effect of differential correlations on information can be detected with relatively simple decoders.

Decision making often involves the accumulation of information over time, but acquiring information typically comes at a cost. Little is known about the cost incurred by animals and humans for acquiring additional information from sensory variables due, for instance, to attentional efforts. Through a novel integration of diffusion models and dynamic programming, we were able to estimate the cost of making additional observations per unit of time from two monkeys and six humans in a reaction time (RT) random-dot motion discrimination task. Surprisingly, we find that the cost is neither zero nor constant over time, but for the animals and humans features a brief period in which it is constant but increases thereafter. In addition, we show that our theory accurately matches the observed reaction time distributions for each stimulus condition, the time-dependent choice accuracy both conditional on stimulus strength and independent of it, and choice accuracy and mean reaction times as a function of stimulus strength. The theory also correctly predicts that urgency signals in the brain should be independent of the difficulty, or stimulus strength, at each trial.

When a stimulus supports two distinct interpretations, perception alternates in an irregular manner between them. What causes the bistable perceptual switches remains an open question. Most existing models assume that switches arise from a slow fatiguing process, such as adaptation or synaptic depression. We develop a new, attractor-based framework in which alternations are induced by noise and are absent without it. Our model goes beyond previous energy-based conceptualizations of perceptual bistability by constructing a neurally plausible attractor model that is implemented in both firing rate mean-field and spiking cell-based networks. The model accounts for known properties of bistable perceptual phenomena, most notably the increase in alternation rate with stimulation strength observed in binocular rivalry. Furthermore, it makes a novel prediction about the effect of changing stimulus strength on the activity levels of the dominant and suppressed neural populations, a prediction that could be tested with functional MRI or electrophysiological recordings. The neural architecture derived from the energy-based model readily generalizes to several competing populations, providing a natural extension for multistability phenomena.

Spike trains from cortical neurons show a high degree of irregularity, with coefficients of variation (CV) of their interspike interval (ISI) distribution close to or higher than one. It has been suggested that this irregularity might be a reflection of a particular dynamical state of the local cortical circuit in which excitation and inhibition balance each other. In this “balanced” state, the mean current to the neurons is below threshold, and firing is driven by current fluctuations, resulting in irregular Poisson-like spike trains. Recent data show that the degree of irregularity in neuronal spike trains recorded during the delay period of working memory experiments is the same for both low-activity states of a few Hz and for elevated, persistent activity states of a few tens of Hz. Since the difference between these persistent activity states cannot be due to external factors coming from sensory inputs, this suggests that the underlying network dynamics might support coexisting balanced states at different firing rates. We use mean field techniques to study the possible existence of multiple balanced steady states in recurrent networks of current-based leaky integrate-and-fire (LIF) neurons. To assess the degree of balance of a steady state, we extend existing mean-field theories so that not only the firing rate, but also the coefficient of variation of the interspike interval distribution of the neurons, are determined self-consistently. Depending on the connectivity parameters of the network, we find bistable solutions of different types. If the local recurrent connectivity is mainly excitatory, the two stable steady states differ mainly in the mean current to the neurons. In this case, the mean drive in the elevated persistent activity state is suprathreshold and typically characterized by low spiking irregularity. If the local recurrent excitatory and inhibitory drives are both large and nearly balanced, or even dominated by inhibition, two stable states coexist, both with subthreshold current drive. In this case, the spiking variability in both the resting state and the mnemonic persistent state is large, but the balance condition implies parameter fine-tuning. Since the degree of required fine-tuning increases with network size and, on the other hand, the size of the fluctuations in the afferent current to the cells increases for small networks, overall we find that fluctuation-driven persistent activity in the very simplified type of models we analyze is not a robust phenomenon. Possible implications of considering more realistic models are discussed.

The brain exhibits complex spatio-temporal patterns of activity. This phenomenon is governed by an interplay between the internal neural dynamics of cortical areas and their connectivity. Uncovering this complex relationship has raised much interest, both for theory and the interpretation of experimental data (e.g., fMRI recordings) using dynamical models. Here we focus on the so-called inverse problem: the inference of network parameters in a cortical model to reproduce empirically observed activity. Although it has received a lot of interest, recovering directed connectivity for large networks has been rather unsuccessful so far. The present study specifically addresses this point for a noise-diffusion network model. We develop a Lyapunov optimization that iteratively tunes the network connectivity in order to reproduce second-order moments of the node activity, or functional connectivity. We show theoretically and numerically that the use of covariances with both zero and non-zero time shifts is the key to infer directed connectivity. The first main theoretical finding is that an accurate estimation of the underlying network connectivity requires that the time shift for covariances is matched with the time constant of the dynamical system. In addition to the network connectivity, we also adjust the intrinsic noise received by each network node. The framework is applied to experimental fMRI data recorded for subjects at rest. Diffusion-weighted MRI data provide an estimate of anatomical connections, which is incorporated to constrain the cortical model. The empirical covariance structure is reproduced faithfully, especially its temporal component (i.e., time-shifted covariances) in addition to the spatial component that is usually the focus of studies. We find that the cortical interactions, referred to as effective connectivity, in the tuned model are not reciprocal. In particular, hubs are either receptors or feeders: they do not exhibit both strong incoming and outgoing connections. Our results sets a quantitative ground to explore the propagation of activity in the cortex. The study of interactions between different cortical regions at rest or during a task has considerably developed in the past decades thanks to progress in non-invasive imaging techniques, such as fMRI, EEG and MEG. These techniques have revealed that distant cortical areas exhibit specific correlated activity during the resting state, also called functional connectivity (FC). Moreover, recent studies have highlighted the possible role of white-matter projections between cortical regions in shaping these activity patterns. This structural connectivity (SC) can be estimated using MRI, which measures the probability for two areas to be connected via the density of neural fibers. However, this does not provide the strengths of dynamical interactions. Many methods have thus been developed to estimate the connectivity between neural populations in the cortex that is hypothesized to shape FC. The strengths of these dynamical interactions are called effective connectivity (EC). We use a cortical model that combines information from Diffusion-weighted MRI (dwMRI) and fMRI in order to estimate EC. We demonstrate theoretically that directed C can be inferred using time-shifted covariances. The key point of our method is the use of temporal information from FC at the scale of the whole network. Applying our model on experimental fMRI data at rest, we estimate the asymmetry of intracortical connectivity. Obtaining an accurate EC estimate is essential to analyze its graph properties, such as hubs. In particular, directed connectivity links to the asymmetry between input and output EC strengths of each node, which characterizes feeder and receiver hubs in the cortical network.