Neuronal Temporal Filters as Normal Mode Extractors

To generate actions in the face of physiological delays, the brain must predict the future. Here we explore how prediction may lie at the core of brain function by considering a neuron predicting the future of a scalar time series input. Assuming that the dynamics of the lag vector (a vector composed of several consecutive elements of the time series) are locally linear, Normal Mode Decomposition decomposes the dynamics into independently evolving (eigen-)modes allowing for straightforward prediction. We propose that a neuron learns the top mode and projects its input onto the associated subspace. Under this interpretation, the temporal filter of a neuron corresponds to the left eigenvector of a generalized eigenvalue problem. We mathematically analyze the operation of such an algorithm on noisy observations of synthetic data generated by a linear system. Interestingly, the shape of the temporal filter varies with the signal-to-noise ratio (SNR): a noisy input yields a monophasic filter and a growing SNR leads to multiphasic filters with progressively greater number of phases. Such variation in the temporal filter with input SNR resembles that observed experimentally in biological neurons.

The Neuron as a Direct Data-Driven Controller

In the quest to model neuronal function amidst gaps in physiological data, a promising strategy is to develop a normative theory that interprets neuronal physiology as optimizing a computational objective. This study extends the current normative models, which primarily optimize prediction, by conceptualizing neurons as optimal feedback controllers. We posit that neurons, especially those beyond early sensory areas, act as controllers, steering their environment towards a specific desired state through their output. This environment comprises both synaptically interlinked neurons and external motor sensory feedback loops, enabling neurons to evaluate the effectiveness of their control via synaptic feedback. Utilizing the novel Direct Data-Driven Control (DD-DC) framework, we model neurons as biologically feasible controllers which implicitly identify loop dynamics, infer latent states and optimize control. Our DD-DC neuron model explains various neurophysiological phenomena: the shift from potentiation to depression in Spike-Timing-Dependent Plasticity (STDP) with its asymmetry, the duration and adaptive nature of feedforward and feedback neuronal filters, the imprecision in spike generation under constant stimulation, and the characteristic operational variability and noise in the brain. Our model presents a significant departure from the traditional, feedforward, instant-response McCulloch-Pitts-Rosenblatt neuron, offering a novel and biologically-informed fundamental unit for constructing neural networks.

Adaptive whitening with fast gain modulation and slow synaptic plasticity

Neurons in early sensory areas rapidly adapt to changing sensory statistics, both by normalizing the variance of their individual responses and by reducing correlations between their responses. Together, these transformations may be viewed as an adaptive form of statistical whitening. Existing mechanistic models of adaptive whitening exclusively use either synaptic plasticity or gain modulation as the biological substrate for adaptation; however, on their own, each of these models has significant limitations. In this work, we unify these approaches in a normative multi-timescale mechanistic model that adaptively whitens its responses with complementary computational roles for synaptic plasticity and gain modulation. Gains are modified on a fast timescale to adapt to the current statistical context, whereas synapses are modified on a slow timescale to learn structural properties of the input statistics that are invariant across contexts. Our model is derived from a novel multi-timescale whitening objective that factorizes the inverse whitening matrix into basis vectors, which correspond to synaptic weights, and a diagonal matrix, which corresponds to neuronal gains. We test our model on synthetic and natural datasets and find that the synapses learn optimal configurations over long timescales that enable the circuit to adaptively whiten neural responses on short timescales exclusively using gain modulation.

Unlocking the Potential of Similarity Matching: Scalability, Supervision and Pre-training

While effective, the backpropagation (BP) algorithm exhibits limitations in terms of biological plausibility, computational cost, and suitability for online learning. As a result, there has been a growing interest in developing alternative biologically plausible learning approaches that rely on local learning rules. This study focuses on the primarily unsupervised similarity matching (SM) framework, which aligns with observed mechanisms in biological systems and offers online, localized, and biologically plausible algorithms. i) To scale SM to large datasets, we propose an implementation of Convolutional Nonnegative SM using PyTorch. ii) We introduce a localized supervised SM objective reminiscent of canonical correlation analysis, facilitating stacking SM layers. iii) We leverage the PyTorch implementation for pre-training architectures such as LeNet and compare the evaluation of features against BP-trained models. This work combines biologically plausible algorithms with computational efficiency opening multiple avenues for further explorations.

A normative framework for deriving neural networks with multi-compartmental neurons and non-Hebbian plasticity

An established normative approach for understanding the algorithmic basis of neural computation is to derive online algorithms from principled computational objectives and evaluate their compatibility with anatomical and physiological observations. Similarity matching objectives have served as successful starting points for deriving online algorithms that map onto neural networks (NNs) with point neurons and Hebbian/anti-Hebbian plasticity. These NN models account for many anatomical and physiological observations; however, the objectives have limited computational power and the derived NNs do not explain multi-compartmental neuronal structures and non-Hebbian forms of plasticity that are prevalent throughout the brain. In this article, we review and unify recent extensions of the similarity matching approach to address more complex objectives, including a broad range of unsupervised and self-supervised learning tasks that can be formulated as generalized eigenvalue problems or nonnegative matrix factorization problems. Interestingly, the online algorithms derived from these objectives naturally map onto NNs with multi-compartmental neurons and local, non-Hebbian learning rules. Therefore, this unified extension of the similarity matching approach provides a normative framework that facilitates understanding the multi-compartmental neuronal structures and non-Hebbian plasticity found throughout the brain.

Statistical whitening of neural populations with gain-modulating interneurons

Statistical whitening transformations play a fundamental role in many computational systems, and may also play an important role in biological sensory systems. Individual neurons appear to rapidly and reversibly alter their input-output gains, approximately normalizing the variance of their responses. Populations of neurons appear to regulate their joint responses, reducing correlations between neural activities. It is natural to see whitening as the objective that guides these behaviors, but the mechanism for such joint changes is unknown, and direct adjustment of synaptic interactions would seem to be both too slow, and insufficiently reversible. Motivated by the extensive neuroscience literature on rapid gain modulation, we propose a recurrent network architecture in which joint whitening is achieved through modulation of gains within the circuit. Specifically, we derive an online statistical whitening algorithm that regulates the joint second-order statistics of a multi-dimensional input by adjusting the marginal variances of an overcomplete set of interneuron projections. The gains of these interneurons are adjusted individually, using only local signals, and feed back onto the primary neurons. The network converges to a state in which the responses of the primary neurons are whitened. We demonstrate through simulations that the behavior of the network is robust to poor conditioning or noise when the gains are sign-constrained, and can be generalized to achieve a form of local whitening in convolutional populations, such as those found throughout the visual or auditory system.

An online algorithm for contrastive Principal Component Analysis

Finding informative low-dimensional representations that can be computed efficiently in large datasets is an important problem in data analysis. Recently, contrastive Principal Component Analysis (cPCA) was proposed as a more informative generalization of PCA that takes advantage of contrastive learning. However, the performance of cPCA is sensitive to hyper-parameter choice and there is currently no online algorithm for implementing cPCA. Here, we introduce a modified cPCA method, which we denote cPCA*, that is more interpretable and less sensitive to the choice of hyper-parameter. We derive an online algorithm for cPCA* and show that it maps onto a neural network with local learning rules, so it can potentially be implemented in energy efficient neuromorphic hardware. We evaluate the performance of our online algorithm on real datasets and highlight the differences and similarities with the original formulation.

Interneurons accelerate learning dynamics in recurrent neural networks for statistical adaptation

Early sensory systems in the brain rapidly adapt to fluctuating input statistics, which requires recurrent communication between neurons. Mechanistically, such recurrent communication is often indirect and mediated by local interneurons. In this work, we explore the computational benefits of mediating recurrent communication via interneurons compared with direct recurrent connections. To this end, we consider two mathematically tractable recurrent neural networks that statistically whiten their inputs -- one with direct recurrent connections and the other with interneurons that mediate recurrent communication. By analyzing the corresponding continuous synaptic dynamics and numerically simulating the networks, we show that the network with interneurons is more robust to initialization than the network with direct recurrent connections in the sense that the convergence time for the synaptic dynamics in the network with interneurons (resp. direct recurrent connections) scales logarithmically (resp. linearly) with the spectrum of their initialization. Our results suggest that interneurons are computationally useful for rapid adaptation to changing input statistics. Interestingly, the network with interneurons is an overparameterized solution of the whitening objective for the network with direct recurrent connections, so our results can be viewed as a recurrent neural network analogue of the implicit acceleration phenomenon observed in overparameterized feedforward linear networks.

Bridging the Gap: Point Clouds for Merging Neurons in Connectomics

In the field of Connectomics, a primary problem is that of 3D neuron segmentation. Although deep learning-based methods have achieved remarkable accuracy, errors still exist, especially in regions with image defects. One common type of defect is that of consecutive missing image sections. Here, data is lost along some axis, and the resulting neuron segmentations are split across the gap. To address this problem, we propose a novel method based on point cloud representations of neurons. We formulate the problem as a classification problem and train CurveNet, a state-of-the-art point cloud classification model, to identify which neurons should be merged. We show that our method not only performs strongly but also scales reasonably to gaps well beyond what other methods have attempted to address. Additionally, our point cloud representations are highly efficient in terms of data, maintaining high performance with an amount of data that would be unfeasible for other methods. We believe that this is an indicator of the viability of using point cloud representations for other proofreading tasks.

Neural optimal feedback control with local learning rules

A major problem in motor control is understanding how the brain plans and executes proper movements in the face of delayed and noisy stimuli. A prominent framework for addressing such control problems is Optimal Feedback Control (OFC). OFC generates control actions that optimize behaviorally relevant criteria by integrating noisy sensory stimuli and the predictions of an internal model using the Kalman filter or its extensions. However, a satisfactory neural model of Kalman filtering and control is lacking because existing proposals have the following limitations: not considering the delay of sensory feedback, training in alternating phases, and requiring knowledge of the noise covariance matrices, as well as that of systems dynamics. Moreover, the majority of these studies considered Kalman filtering in isolation, and not jointly with control. To address these shortcomings, we introduce a novel online algorithm which combines adaptive Kalman filtering with a model free control approach (i.e., policy gradient algorithm). We implement this algorithm in a biologically plausible neural network with local synaptic plasticity rules. This network performs system identification and Kalman filtering, without the need for multiple phases with distinct update rules or the knowledge of the noise covariances. It can perform state estimation with delayed sensory feedback, with the help of an internal model. It learns the control policy without requiring any knowledge of the dynamics, thus avoiding the need for weight transport. In this way, our implementation of OFC solves the credit assignment problem needed to produce the appropriate sensory-motor control in the presence of stimulus delay.