Order from chaos: Interplay of development and learning in recurrent networks of structured neurons

Behavior can be described as a temporal sequence of actions driven by neural activity. To learn complex sequential patterns in neural networks, memories of past activities need to persist on significantly longer timescales than relaxation times of single-neuron activity. While recurrent networks can produce such long transients, training these networks in a biologically plausible way is challenging. One approach has been reservoir computing, where only weights from a recurrent network to a readout are learned. Other models achieve learning of recurrent synaptic weights using propagated errors. However, their biological plausibility typically suffers from issues with locality, resource allocation or parameter scales and tuning. We suggest that many of these issues can be alleviated by considering dendritic information storage and computation. By applying a fully local, always-on plasticity rule we are able to learn complex sequences in a recurrent network comprised of two populations. Importantly, our model is resource-efficient, enabling the learning of complex sequences using only a small number of neurons. We demonstrate these features in a mock-up of birdsong learning, in which our networks first learn a long, non-Markovian sequence that they can then reproduce robustly despite external disturbances.

Precision estimation and second-order prediction errors in cortical circuits

Minimization of cortical prediction errors is believed to be a key canonical computation of the cerebral cortex underlying perception, action and learning. However, it is still unclear how the cortex should form and use knowledge about uncertainty in this process of prediction error minimization. Here we derive neural dynamics minimizing prediction errors under the assumption that cortical areas must not only predict the activity in other areas and sensory streams, but also jointly estimate the precision of their predictions. This leads to a dynamic modulatory balancing of cortical streams based on context-dependent precision estimates. Moreover, the theory predicts the existence of second-order prediction errors, i.e. errors on precision estimates, computed and propagated through the cortical hierarchy alongside classical prediction errors. These second-order errors are used to learn weights of synapses responsible for precision estimation through an error-correcting synaptic learning rule. Finally, we propose a mapping of the theory to cortical circuitry.

Learning beyond sensations: how dreams organize neuronal representations

Semantic representations in higher sensory cortices form the basis for robust, yet flexible behavior. These representations are acquired over the course of development in an unsupervised fashion and continuously maintained over an organism's lifespan. Predictive learning theories propose that these representations emerge from predicting or reconstructing sensory inputs. However, brains are known to generate virtual experiences, such as during imagination and dreaming, that go beyond previously experienced inputs. Here, we suggest that virtual experiences may be just as relevant as actual sensory inputs in shaping cortical representations. In particular, we discuss two complementary learning principles that organize representations through the generation of virtual experiences. First, "adversarial dreaming" proposes that creative dreams support a cortical implementation of adversarial learning in which feedback and feedforward pathways engage in a productive game of trying to fool each other. Second, "contrastive dreaming" proposes that the invariance of neuronal representations to irrelevant factors of variation is acquired by trying to map similar virtual experiences together via a contrastive learning process. These principles are compatible with known cortical structure and dynamics and the phenomenology of sleep thus providing promising directions to explain cortical learning beyond the classical predictive learning paradigm.

Learning efficient backprojections across cortical hierarchies in real time

Models of sensory processing and learning in the cortex need to efficiently assign credit to synapses in all areas. In deep learning, a known solution is error backpropagation, which however requires biologically implausible weight transport from feed-forward to feedback paths. We introduce Phaseless Alignment Learning (PAL), a bio-plausible method to learn efficient feedback weights in layered cortical hierarchies. This is achieved by exploiting the noise naturally found in biophysical systems as an additional carrier of information. In our dynamical system, all weights are learned simultaneously with always-on plasticity and using only information locally available to the synapses. Our method is completely phase-free (no forward and backward passes or phased learning) and allows for efficient error propagation across multi-layer cortical hierarchies, while maintaining biologically plausible signal transport and learning. Our method is applicable to a wide class of models and improves on previously known biologically plausible ways of credit assignment: compared to random synaptic feedback, it can solve complex tasks with less neurons and learn more useful latent representations. We demonstrate this on various classification tasks using a cortical microcircuit model with prospective coding.

Latent Equilibrium: A unified learning theory for arbitrarily fast computation with arbitrarily slow neurons

The response time of physical computational elements is finite, and neurons are no exception. In hierarchical models of cortical networks each layer thus introduces a response lag. This inherent property of physical dynamical systems results in delayed processing of stimuli and causes a timing mismatch between network output and instructive signals, thus afflicting not only inference, but also learning. We introduce Latent Equilibrium, a new framework for inference and learning in networks of slow components which avoids these issues by harnessing the ability of biological neurons to phase-advance their output with respect to their membrane potential. This principle enables quasi-instantaneous inference independent of network depth and avoids the need for phased plasticity or computationally expensive network relaxation phases. We jointly derive disentangled neuron and synapse dynamics from a prospective energy function that depends on a network's generalized position and momentum. The resulting model can be interpreted as a biologically plausible approximation of error backpropagation in deep cortical networks with continuous-time, leaky neuronal dynamics and continuously active, local plasticity. We demonstrate successful learning of standard benchmark datasets, achieving competitive performance using both fully-connected and convolutional architectures, and show how our principle can be applied to detailed models of cortical microcircuitry. Furthermore, we study the robustness of our model to spatio-temporal substrate imperfections to demonstrate its feasibility for physical realization, be it in vivo or in silico.

Memory semantization through perturbed and adversarial dreaming

Classical theories of memory consolidation emphasize the importance of replay in extracting semantic information from episodic memories. However, the characteristic creative nature of dreams suggests that memory semantization may go beyond merely replaying previous experiences. We propose that rapid-eye-movement (REM) dreaming is essential for efficient memory semantization by randomly combining episodic memories to create new, virtual sensory experiences. We support this hypothesis by implementing a cortical architecture with hierarchically organized feedforward and feedback pathways, inspired by generative adversarial networks (GANs). Learning in our model is organized across three different global brain states mimicking wakefulness, non-REM (NREM) and REM sleep, optimizing different, but complementary objective functions. We train the model in an unsupervised fashion on standard datasets of natural images and evaluate the quality of the learned representations. Our results suggest that adversarial dreaming during REM sleep is essential for extracting memory contents, while perturbed dreaming during NREM sleep improves robustness of the latent representation to noisy sensory inputs. The model provides a new computational perspective on sleep states, memory replay and dreams and suggests a cortical implementation of GANs.

Evolving Neuronal Plasticity Rules using Cartesian Genetic Programming

We formulate the search for phenomenological models of synaptic plasticity as an optimization problem. We employ Cartesian genetic programming to evolve biologically plausible human-interpretable plasticity rules that allow a given network to successfully solve tasks from specific task families. While our evolving-to-learn approach can be applied to various learning paradigms, here we illustrate its power by evolving plasticity rules that allow a network to efficiently determine the first principal component of its input distribution. We demonstrate that the evolved rules perform competitively with known hand-designed solutions. We explore how the statistical properties of the datasets used during the evolutionary search influences the form of the plasticity rules and discover new rules which are adapted to the structure of the corresponding datasets.

Versatile emulation of spiking neural networks on an accelerated neuromorphic substrate

We present first experimental results on the novel BrainScaleS-2 neuromorphic architecture based on an analog neuro-synaptic core and augmented by embedded microprocessors for complex plasticity and experiment control. The high acceleration factor of 1000 compared to biological dynamics enables the execution of computationally expensive tasks, by allowing the fast emulation of long-duration experiments or rapid iteration over many consecutive trials. The flexibility of our architecture is demonstrated in a suite of five distinct experiments, which emphasize different aspects of the BrainScaleS-2 system.

Fast and deep neuromorphic learning with time-to-first-spike coding

For a biological agent operating under environmental pressure, energy consumption and reaction times are of critical importance. Similarly, engineered systems also strive for short time-to-solution and low energy-to-solution characteristics. At the level of neuronal implementation, this implies achieving the desired results with as few and as early spikes as possible. In the time-to-first-spike coding framework, both of these goals are inherently emerging features of learning. Here, we describe a rigorous derivation of error-backpropagation-based learning for hierarchical networks of leaky integrate-and-fire neurons. We explicitly address two issues that are relevant for both biological plausibility and applicability to neuromorphic substrates by incorporating dynamics with finite time constants and by optimizing the backward pass with respect to substrate variability. This narrows the gap between previous models of first-spike-time learning and biological neuronal dynamics, thereby also enabling fast and energy-efficient inference on analog neuromorphic devices that inherit these dynamics from their biological archetypes, which we demonstrate on two generations of the BrainScaleS analog neuromorphic architecture.

Ghost Units Yield Biologically Plausible Backprop in Deep Neural Networks

In the past few years, deep learning has transformed artificial intelligence research and led to impressive performance in various difficult tasks. However, it is still unclear how the brain can perform credit assignment across many areas as efficiently as backpropagation does in deep neural networks. In this paper, we introduce a model that relies on a new role for a neuronal inhibitory machinery, referred to as ghost units. By cancelling the feedback coming from the upper layer when no target signal is provided to the top layer, the ghost units enables the network to backpropagate errors and do efficient credit assignment in deep structures. While considering one-compartment neurons and requiring very few biological assumptions, it is able to approximate the error gradient and achieve good performance on classification tasks. Error backpropagation occurs through the recurrent dynamics of the network and thanks to biologically plausible local learning rules. In particular, it does not require separate feedforward and feedback circuits. Different mechanisms for cancelling the feedback were studied, ranging from complete duplication of the connectivity by long term processes to online replication of the feedback activity. This reduced system combines the essential elements to have a working biologically abstracted analogue of backpropagation with a simple formulation and proofs of the associated results. Therefore, this model is a step towards understanding how learning and memory are implemented in cortical multilayer structures, but it also raises interesting perspectives for neuromorphic hardware.