arXiv subjects

Ulisse Ferrari

Publications and source records attributed to Ulisse Ferrari.

At least 19 recordsLinked to original sources

arXiv2026

A multi-scale information geometry reveals the structure of mutual information in neural populations

Understanding how neural population responses represent sensory information is a central problem in systems neuroscience. One approach is to define a representational geometry on stimulus space in which distances reflect how reliably stimuli can be distinguished from neural activity. However, different constructions of these distances can lead to qualitatively different conclusions about the neural code. Here, we show that a unique Riemannian representational geometry emerges from first principles governing how distances contract as stimulus resolution is lost through coarse-graining. This results in a multi-scale extension of the Fisher information metric, capturing encoding structure from fine stimulus details to coarse global distinctions. The resulting geometry is exactly related to the mutual information encoded by the population: well encoded stimulus directions - those contributing more to mutual information - are expanded, whereas poorly encoded directions are contracted. The metric tensor can be estimated using diffusion models, making the framework practical for large neural populations and high-dimensional stimuli. Applied to visual cortical responses to natural images, the eigenvectors of the metric tensor identify stimulus variations that contribute most to information transmission, yielding interpretable features that are robust to modelling choices. Together, these results provide a principled, information-theoretic framework for characterising neural population codes.

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arXiv2025

Decomposing stimulus-specific sensory neural information via diffusion models

To understand sensory coding, we must ask not only how much information neurons encode, but also what that information is about. This requires decomposing mutual information into contributions from individual stimuli and stimulus features: a fundamentally ill-posed problem with infinitely many possible solutions. We address this by introducing three core axioms, additivity, positivity, and locality that any meaningful stimulus-wise decomposition should satisfy. We then derive a decomposition that meets all three criteria and remains tractable for high-dimensional stimuli. Our decomposition can be efficiently estimated using diffusion models, allowing for scaling up to complex, structured and naturalistic stimuli. Applied to a model of visual neurons, our method quantifies how specific stimuli and features contribute to encoded information. Our approach provides a scalable, interpretable tool for probing representations in both biological and artificial neural systems.

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arXiv2025

Higher-Order Convolution Improves Neural Predictivity in the Retina

We present a novel approach to neural response prediction that incorporates higher-order operations directly within convolutional neural networks (CNNs). Our model extends traditional 3D CNNs by embedding higher-order operations within the convolutional operator itself, enabling direct modeling of multiplicative interactions between neighboring pixels across space and time. Our model increases the representational power of CNNs without increasing their depth, therefore addressing the architectural disparity between deep artificial networks and the relatively shallow processing hierarchy of biological visual systems. We evaluate our approach on two distinct datasets: salamander retinal ganglion cell (RGC) responses to natural scenes, and a new dataset of mouse RGC responses to controlled geometric transformations. Our higher-order CNN (HoCNN) achieves superior performance while requiring only half the training data compared to standard architectures, demonstrating correlation coefficients up to 0.75 with neural responses (against 0.80$\pm$0.02 retinal reliability). When integrated into state-of-the-art architectures, our approach consistently improves performance across different species and stimulus conditions. Analysis of the learned representations reveals that our network naturally encodes fundamental geometric transformations, particularly scaling parameters that characterize object expansion and contraction. This capability is especially relevant for specific cell types, such as transient OFF-alpha and transient ON cells, which are known to detect looming objects and object motion respectively, and where our model shows marked improvement in response prediction. The correlation coefficients for scaling parameters are more than twice as high in HoCNN (0.72) compared to baseline models (0.32).

cs.CV↗

arXiv2025

Diagrammatic expansion for the mutual-information rate in the realm of limited statistics

Neurons in sensory systems encode stimulus information into their stochastic spiking response. The mutual information has been extensively applied to these systems to quantify the neurons' capacity of transmitting such information. Yet, while for discrete stimuli, like flashed images or single tones, its computation is straightforward, for dynamical stimuli it is necessary to compute a (mutual) information rate (MIR), therefore integrating over the multiple temporal correlations which characterize sensory systems. Previous methods are based on extensive sampling of the neuronal response, require large amounts of data and are therefore prone to biases and inaccuracy. Here, we develop Moba-MIRA (moment-based mutual-information-rate approximation), a computational method to estimate the mutual information rate. To derive Moba-MIRA, we use Feynman diagrams to expand the mutual information to arbitrary order in the correlations around the corresponding value for the empirical spike count distributions of single bins. As a result, only the empirical estimation of the pairwise correlations between time bins and the single-bin entropies are required, without the need for the whole joint probability distributions. We tested Moba-MIRA on synthetic data generated with generalized linear models, and showed that it requires only a few tens of stimulus repetitions to provide an accurate estimate of the information rate. Finally, we applied it to ex-vivo electrophysiological recordings of rats retina, obtaining rates ranging between 5 to 20 bits per second, consistent with earlier estimates.

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arXiv2024

Convolution goes higher-order: a biologically inspired mechanism empowers image classification

We propose a novel approach to image classification inspired by complex nonlinear biological visual processing, whereby classical convolutional neural networks (CNNs) are equipped with learnable higher-order convolutions. Our model incorporates a Volterra-like expansion of the convolution operator, capturing multiplicative interactions akin to those observed in early and advanced stages of biological visual processing. We evaluated this approach on synthetic datasets by measuring sensitivity to testing higher-order correlations and performance in standard benchmarks (MNIST, FashionMNIST, CIFAR10, CIFAR100 and Imagenette). Our architecture outperforms traditional CNN baselines, and achieves optimal performance with expansions up to 3rd/4th order, aligning remarkably well with the distribution of pixel intensities in natural images. Through systematic perturbation analysis, we validate this alignment by isolating the contributions of specific image statistics to model performance, demonstrating how different orders of convolution process distinct aspects of visual information. Furthermore, Representational Similarity Analysis reveals distinct geometries across network layers, indicating qualitatively different modes of visual information processing. Our work bridges neuroscience and deep learning, offering a path towards more effective, biologically inspired computer vision models. It provides insights into visual information processing and lays the groundwork for neural networks that better capture complex visual patterns, particularly in resource-constrained scenarios.

cs.CV↗

arXiv2024

Strong, but not weak, noise correlations are beneficial for population coding

Neural correlations play a critical role in sensory information coding. They are of two kinds: signal correlations, when neurons have overlapping sensitivities, and noise correlations from network effects and shared noise. In experiments from early sensory systems and cortex, many pairs of neurons typically show both types of correlations to be positive and large, especially between nearby neurons with similar stimulus sensitivity. However, theoretical arguments have suggested that stimulus and noise correlations should have opposite signs to improve coding, at odds with experimental observations. We analyze retinal recording in response to a large variety of stimuli, and show that, contrary to common belief, large noise correlations are beneficial for coding, even if aligned with signal correlations. To understand this result, we develop a theory of visual information coding by correlated neurons, which resolves that paradox. We show that noise correlations are always beneficial if they are strong enough, unless neurons are perfectly correlated by the stimulus. Finally, using neuronal recordings and modeling, we show that for high dimensional stimuli noise correlation benefits the encoding of fine-grained details of visual stimuli, at the expense of large-scale features, which are already well encoded.

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arXiv2022

A small-correlation expansion to quantify information in noisy sensory systems

Neural networks encode information through their collective spiking activity in response to external stimuli. This population response is noisy and strongly correlated, with complex interplay between correlations induced by the stimulus, and correlations caused by shared noise. Understanding how these correlations affect information transmission has so far been limited to pairs or small groups of neurons, because the curse of dimensionality impedes the evaluation of mutual information in larger populations. Here we develop a small-correlation expansion to compute the stimulus information carried by a large population of neurons, yielding interpretable analytical expressions in terms of the neurons' firing rates and pairwise correlations. We validate the approximation on synthetic data and demonstrate its applicability to electrophysiological recordings in the vertebrate retina, allowing us to quantify the effects of noise correlations between neurons and of memory in single neurons.

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arXiv2022

Time-dependent maximum entropy model for populations of retinal ganglion cells

The inverse Ising model is used in computational neuroscience to infer probability distributions of the synchronous activity of large neuronal populations. This method allows for finding the Boltzmann distribution with single neuron biases and pairwise interactions that maximizes the entropy and reproduces the empirical statistics of the recorded neuronal activity. Here we apply this strategy to large populations of retinal output neurons (ganglion cells) of different types, stimulated by multiple visual stimuli with their own statistics. The activity of retinal output neurons is driven by both the inputs from upstream neurons and the recurrent connections. We first apply the standard inverse Ising model approach, and show that it accounts well for the system's collective behavior when the input visual stimulus has short-ranged spatial correlations, but fails for long-ranged ones. This happens because stimuli with long-ranged spatial correlations synchronize the activity of neurons over long distances. This effect cannot be accounted for by pairwise interactions, and so by the pairwise Ising model. To solve this issue, we apply a previously proposed framework that includes a temporal dependence in the single neurons biases to model how neurons are driven in time by the stimulus. Thanks to this addition, the stimulus effects are taken into account by the biases, and the pairwise interactions allow for characterizing the network effect in the population activity and for reproducing the structure of the recurrent functional connections in the retinal architecture. We found that the retinal architecture splits into weakly interacting subpopulations composed of strongly interacting neurons. Overall, this temporal framework fixes the problems of the standard, static, inverse Ising model and accounts for the system's collective behavior, for stimuli with either short or long-range correlations.

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arXiv2020

A new inference approach for training shallow and deep generalized linear models of noisy interacting neurons

Generalized linear models are one of the most efficient paradigms for predicting the correlated stochastic activity of neuronal networks in response to external stimuli, with applications in many brain areas. However, when dealing with complex stimuli, the inferred coupling parameters often do not generalize across different stimulus statistics, leading to degraded performance and blowup instabilities. Here, we develop a two-step inference strategy that allows us to train robust generalized linear models of interacting neurons, by explicitly separating the effects of correlations in the stimulus from network interactions in each training step. Applying this approach to the responses of retinal ganglion cells to complex visual stimuli, we show that, compared to classical methods, the models trained in this way exhibit improved performance, are more stable, yield robust interaction networks, and generalize well across complex visual statistics. The method can be extended to deep convolutional neural networks, leading to models with high predictive accuracy for both the neuron firing rates and their correlations.

cond-mat.dis-nn↗

arXiv2019

Cholinergic switch between two types of slow waves in cerebral cortex

Sleep slow waves are known to participate in memory consolidation, yet slow waves occurring under anesthesia present no positive effects on memory. Here, we shed light onto this paradox, based on a combination of extracellular recordings in vivo, in vitro, and computational models. We find two types of slow waves, based on analyzing the temporal patterns of successive slow-wave events. The first type is consistently observed in natural slow-wave sleep, while the second is shown to be ubiquitous under anesthesia. Network models of spiking neurons predict that the two slow wave types emerge due to a different gain on inhibitory vs excitatory cells and that different levels of spike-frequency adaptation in excitatory cells can account for dynamical distinctions between the two types. This prediction was tested in vitro by varying adaptation strength using an agonist of acetylcholine receptors, which demonstrated a neuromodulatory switch between the two types of slow waves. Finally, we show that the first type of slow-wave dynamics is more sensitive to external stimuli, which can explain how slow waves in sleep and anesthesia differentially affect memory consolidation, as well as provide a link between slow-wave dynamics and memory diseases.

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arXiv2019

Predicting synchronous firing of large neural populations from sequential recordings

A major goal in neuroscience is to understand how populations of neurons code for stimuli or actions. While the number of neurons that can be recorded simultaneously is increasing at a fast pace, in most cases these recordings cannot access a complete population. In particular, it is hard to simultaneously record all the neurons of the same type in a given area. Recent progress have made possible to profile each recorded neuron in a given area thanks to genetic and physiological tools, and to pool together recordings from neurons of the same type across different experimental sessions. However, it is unclear how to infer the activity of a full population of neurons of the same type from these sequential recordings. Neural networks exhibit collective behaviour, e.g. noise correlations and synchronous activity, that are not directly captured by a conditionally-independent model that would just put together the spike trains from sequential recordings. Here we show that we can infer the activity of a full population of retina ganglion cells from sequential recordings, using a novel method based on copula distributions and maximum entropy modeling. From just the spiking response of each ganglion cell to a repeated stimulus, and a few pairwise recordings, we could predict the noise correlations using copulas, and then the full activity of a large population of ganglion cells of the same type using maximum entropy modeling. Remarkably, we could generalize to predict the population responses to different stimuli and even to different experiments. We could therefore use our method to construct a very large population merging cells' responses from different experiments. We predicted synchronous activity accurately and showed it grew substantially with the number of neurons. This approach is a promising way to infer population activity from sequential recordings in sensory areas.

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arXiv2018

Optogenetic vision restoration with high resolution

The majority of inherited retinal degenerations are due to photoreceptor cell death. In many cases ganglion cells are spared making it possible to stimulate them to restore visual function. Several studies (Bi et al., 2006; Lin et al., 2008; Sengupta et al., 2016; Caporale et al., 2011; Berry et al., 2017) have shown that it is possible to express an optogenetic protein in ganglion cells and make them light sensitive. This is a promising strategy to restore vision since optical targeting may be more precise than electrical stimulation with a retinal prothesis. However the spatial resolution of optogenetically-reactivated retinas has not been measured with fine-grained stimulation patterns. Since the optogenetic protein is also expressed in axons, it is unclear if these neurons will only be sensitive to the stimulation of a small region covering their somas and dendrites, or if they will also respond to any stimulation overlapping with their axon, dramatically impairing spatial resolution. Here we recorded responses of mouse and macaque retinas to random checkerboard patterns following an in vivo optogenetic therapy. We show that optogenetically activated ganglion cells are each sensitive to a small region of visual space. A simple model based on this small receptive field predicted accurately their responses to complex stimuli. From this model, we simulated how the entire population of light sensitive ganglion cells would respond to letters of different sizes. We then estimated the maximal acuity expected by a patient, assuming it could make an optimal use of the information delivered by this reactivated retina. The obtained acuity is above the limit of legal blindness. This high spatial resolution is a promising result for future clinical studies.

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arXiv2018

Maximum entropy models reveal the excitatory and inhibitory correlation structures in cortical neuronal activity

Maximum Entropy models can be inferred from large data-sets to uncover how collective dynamics emerge from local interactions. Here, such models are employed to investigate neurons recorded by multielectrode arrays in the human and monkey cortex. Taking advantage of the separation of excitatory and inhibitory neuron types, we construct a model including this distinction. This approach allows to shed light upon differences between excitatory and inhibitory activity across different brain states such as wakefulness and deep sleep, in agreement with previous findings. Additionally, Maximum Entropy models can also unveil novel features of neuronal interactions, which are found to be dominated by pairwise interactions during wakefulness, but are population-wide during deep sleep. In particular, inhibitory neurons are observed to be strongly tuned to the inhibitory population. Overall, we demonstrate Maximum Entropy models can be useful to analyze data-sets with classified neuron types, and to reveal the respective roles of excitatory and inhibitory neurons in organizing coherent dynamics in the cerebral cortex.

q-bio.NC↗

arXiv2018

Separating intrinsic interactions from extrinsic correlations in a network of sensory neurons

Correlations in sensory neural networks have both extrinsic and intrinsic origins. Extrinsic or stimulus correlations arise from shared inputs to the network, and thus depend strongly on the stimulus ensemble. Intrinsic or noise correlations reflect biophysical mechanisms of interactions between neurons, which are expected to be robust to changes of the stimulus ensemble. Despite the importance of this distinction for understanding how sensory networks encode information collectively, no method exists to reliably separate intrinsic interactions from extrinsic correlations in neural activity data, limiting our ability to build predictive models of the network response. In this paper we introduce a general strategy to infer {population models of interacting neurons that collectively encode stimulus information}. The key to disentangling intrinsic from extrinsic correlations is to infer the {couplings between neurons} separately from the encoding model, and to combine the two using corrections calculated in a mean-field approximation. We demonstrate the effectiveness of this approach on retinal recordings. The same coupling network is inferred from responses to radically different stimulus ensembles, showing that these couplings indeed reflect stimulus-independent interactions between neurons. The inferred model predicts accurately the collective response of retinal ganglion cell populations as a function of the stimulus.

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arXiv2018

A simple model for low variability in neural spike trains

Neural noise sets a limit to information transmission in sensory systems. In several areas, the spiking response (to a repeated stimulus) has shown a higher degree of regularity than predicted by a Poisson process. However, a simple model to explain this low variability is still lacking. Here we introduce a new model, with a correction to Poisson statistics, which can accurately predict the regularity of neural spike trains in response to a repeated stimulus. The model has only two parameters, but can reproduce the observed variability in retinal recordings in various conditions. We show analytically why this approximation can work. In a model of the spike emitting process where a refractory period is assumed, we derive that our simple correction can well approximate the spike train statistics over a broad range of firing rates. Our model can be easily plugged to stimulus processing models, like Linear-nonlinear model or its generalizations, to replace the Poisson spike train hypothesis that is commonly assumed. It estimates the amount of information transmitted much more accurately than Poisson models in retinal recordings. Thanks to its simplicity this model has the potential to explain low variability in other areas.

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arXiv2017

Pairwise Ising model analysis of human cortical neuron recordings

During wakefulness and deep sleep brain states, cortical neural networks show a different behavior, with the second characterized by transients of high network activity. To investigate their impact on neuronal behavior, we apply a pairwise Ising model analysis by inferring the maximum entropy model that reproduces single and pairwise moments of the neuron's spiking activity. In this work we first review the inference algorithm introduced in Ferrari,Phys. Rev. E (2016). We then succeed in applying the algorithm to infer the model from a large ensemble of neurons recorded by multi-electrode array in human temporal cortex. We compare the Ising model performance in capturing the statistical properties of the network activity during wakefulness and deep sleep. For the latter, the pairwise model misses relevant transients of high network activity, suggesting that additional constraints are necessary to accurately model the data.

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arXiv2017

Closed-loop estimation of retinal network sensitivity reveals signature of efficient coding

According to the theory of efficient coding, sensory systems are adapted to represent natural scenes with high fidelity and at minimal metabolic cost. Testing this hypothesis for sensory structures performing non-linear computations on high dimensional stimuli is still an open challenge. Here we develop a method to characterize the sensitivity of the retinal network to perturbations of a stimulus. Using closed-loop experiments, we explore selectively the space of possible perturbations around a given stimulus. We then show that the response of the retinal population to these small perturbations can be described by a local linear model. Using this model, we computed the sensitivity of the neural response to arbitrary temporal perturbations of the stimulus, and found a peak in the sensitivity as a function of the frequency of the perturbations. Based on a minimal theory of sensory processing, we argue that this peak is set to maximize information transmission. Our approach is relevant to testing the efficient coding hypothesis locally in any context where no reliable encoding model is known.

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arXiv2016

Random versus maximum entropy models of neural population activity

The principle of maximum entropy provides a useful method for inferring statistical mechanics models from observations in correlated systems, and is widely used in a variety of fields where accurate data are available. While the assumptions underlying maximum entropy are intuitive and appealing, its adequacy for describing complex empirical data has been little studied in comparison to alternative approaches. Here data from the collective spiking activity of retinal neurons is reanalysed. The accuracy of the maximum entropy distribution constrained by mean firing rates and pairwise correlations is compared to a random ensemble of distributions constrained by the same observables. In general, maximum entropy approximates the true distribution better than the typical or mean distribution from that ensemble. This advantage improves with population size, with groups as small as 8 being almost always better described by maximum entropy. Failure of maximum entropy to outperform random models is found to be associated with strong correlations in the population.

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