Modular-integrative modeling: a new framework for building brain models that blend biological realism and functional performance.

This Perspective presents the Modular-Integrative Modeling approach, a novel framework in neuroscience for developing brain models that blend biological realism with functional performance to provide a holistic view on brain function in interaction with the body and environment.

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 processing 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 processing paradigm.

Variational learning of quantum ground states on spiking neuromorphic hardware.

Recent research has demonstrated the usefulness of neural networks as variational ansatz functions for quantum many-body states. However, high-dimensional sampling spaces and transient autocorrelations confront these approaches with a challenging computational bottleneck. Compared to conventional neural networks, physical model devices offer a fast, efficient and inherently parallel substrate capable of related forms of Markov chain Monte Carlo sampling. Here, we demonstrate the ability of a neuromorphic chip to represent the ground states of quantum spin models by variational energy minimization. We develop a training algorithm and apply it to the transverse field Ising model, showing good performance at moderate system sizes ( N ≤ 10 ). A systematic hyperparameter study shows that performance depends on sample quality, which is limited by temporal parameter variations on the analog neuromorphic chip. Our work thus provides an important step towards harnessing the capabilities of neuromorphic hardware for tackling the curse of dimensionality in quantum many-body problems.

Natural-gradient learning for spiking neurons.

In many normative theories of synaptic plasticity, weight updates implicitly depend on the chosen parametrization of the weights. This problem relates, for example, to neuronal morphology: synapses which are functionally equivalent in terms of their impact on somatic firing can differ substantially in spine size due to their different positions along the dendritic tree. Classical theories based on Euclidean-gradient descent can easily lead to inconsistencies due to such parametrization dependence. The issues are solved in the framework of Riemannian geometry, in which we propose that plasticity instead follows natural-gradient descent. Under this hypothesis, we derive a synaptic learning rule for spiking neurons that couples functional efficiency with the explanation of several well-documented biological phenomena such as dendritic democracy, multiplicative scaling, and heterosynaptic plasticity. We therefore suggest that in its search for functional synaptic plasticity, evolution might have come up with its own version of natural-gradient descent.

Learning cortical representations through perturbed and adversarial dreaming.

Humans and other animals learn to extract general concepts from sensory experience without extensive teaching. This ability is thought to be facilitated by offline states like sleep where previous experiences are systemically replayed. However, the characteristic creative nature of dreams suggests that learning semantic representations may go beyond merely replaying previous experiences. We support this hypothesis by implementing a cortical architecture inspired by generative adversarial networks (GANs). Learning in our model is organized across three different global brain states mimicking wakefulness, non-rapid eye movement (NREM), and REM sleep, optimizing different, but complementary, objective functions. We train the model on standard datasets of natural images and evaluate the quality of the learned representations. Our results suggest that generating new, virtual sensory inputs via adversarial dreaming during REM sleep is essential for extracting semantic concepts, while replaying episodic memories via perturbed dreaming during NREM sleep improves the robustness of latent representations. The model provides a new computational perspective on sleep states, memory replay, and dreams, and suggests a cortical implementation of GANs.

Cortical oscillations support sampling-based computations in spiking neural networks.

Being permanently confronted with an uncertain world, brains have faced evolutionary pressure to represent this uncertainty in order to respond appropriately. Often, this requires visiting multiple interpretations of the available information or multiple solutions to an encountered problem. This gives rise to the so-called mixing problem: since all of these "valid" states represent powerful attractors, but between themselves can be very dissimilar, switching between such states can be difficult. We propose that cortical oscillations can be effectively used to overcome this challenge. By acting as an effective temperature, background spiking activity modulates exploration. Rhythmic changes induced by cortical oscillations can then be interpreted as a form of simulated tempering. We provide a rigorous mathematical discussion of this link and study some of its phenomenological implications in computer simulations. This identifies a new computational role of cortical oscillations and connects them to various phenomena in the brain, such as sampling-based probabilistic inference, memory replay, multisensory cue combination, and place cell flickering.

Evolving interpretable plasticity for spiking networks.

Continuous adaptation allows survival in an ever-changing world. Adjustments in the synaptic coupling strength between neurons are essential for this capability, setting us apart from simpler, hard-wired organisms. How these changes can be mathematically described at the phenomenological level, as so-called 'plasticity rules', is essential both for understanding biological information processing and for developing cognitively performant artificial systems. We suggest an automated approach for discovering biophysically plausible plasticity rules based on the definition of task families, associated performance measures and biophysical constraints. By evolving compact symbolic expressions, we ensure the discovered plasticity rules are amenable to intuitive understanding, fundamental for successful communication and human-guided generalization. We successfully apply our approach to typical learning scenarios and discover previously unknown mechanisms for learning efficiently from rewards, recover efficient gradient-descent methods for learning from target signals, and uncover various functionally equivalent STDP-like rules with tuned homeostatic mechanisms.

Our brains are incredibly adaptive. Every day we form memories, acquire new knowledge or refine existing skills. This stands in contrast to our current computers, which typically can only perform pre-programmed actions. Our own ability to adapt is the result of a process called synaptic plasticity, in which the strength of the connections between neurons can change. To better understand brain function and build adaptive machines, researchers in neuroscience and artificial intelligence (AI) are modeling the underlying mechanisms. So far, most work towards this goal was guided by human intuition ­ that is, by the strategies scientists think are most likely to succeed. Despite the tremendous progress, this approach has two drawbacks. First, human time is limited and expensive. And second, researchers have a natural ­ and reasonable ­ tendency to incrementally improve upon existing models, rather than starting from scratch. Jordan, Schmidt et al. have now developed a new approach based on 'evolutionary algorithms'. These computer programs search for solutions to problems by mimicking the process of biological evolution, such as the concept of survival of the fittest. The approach exploits the increasing availability of cheap but powerful computers. Compared to its predecessors (or indeed human brains), it also uses search strategies that are less biased by previous models. The evolutionary algorithms were presented with three typical learning scenarios. In the first, the computer had to spot a repeating pattern in a continuous stream of input without receiving feedback on how well it was doing. In the second scenario, the computer received virtual rewards whenever it behaved in the desired manner ­ an example of reinforcement learning. Finally, in the third 'supervised learning' scenario, the computer was told exactly how much its behavior deviated from the desired behavior. For each of these scenarios, the evolutionary algorithms were able to discover mechanisms of synaptic plasticity to solve the new task successfully. Using evolutionary algorithms to study how computers 'learn' will provide new insights into how brains function in health and disease. It could also pave the way for developing intelligent machines that can better adapt to the needs of their users.

Predictive olfactory learning in Drosophila.

Olfactory learning and conditioning in the fruit fly is typically modelled by correlation-based associative synaptic plasticity. It was shown that the conditioning of an odor-evoked response by a shock depends on the connections from Kenyon cells (KC) to mushroom body output neurons (MBONs). Although on the behavioral level conditioning is recognized to be predictive, it remains unclear how MBONs form predictions of aversive or appetitive values (valences) of odors on the circuit level. We present behavioral experiments that are not well explained by associative plasticity between conditioned and unconditioned stimuli, and we suggest two alternative models for how predictions can be formed. In error-driven predictive plasticity, dopaminergic neurons (DANs) represent the error between the predictive odor value and the shock strength. In target-driven predictive plasticity, the DANs represent the target for the predictive MBON activity. Predictive plasticity in KC-to-MBON synapses can also explain trace-conditioning, the valence-dependent sign switch in plasticity, and the observed novelty-familiarity representation. The model offers a framework to dissect MBON circuits and interpret DAN activity during olfactory learning.

Visualizing a joint future of neuroscience and neuromorphic engineering.

Recent research resolves the challenging problem of building biophysically plausible spiking neural models that are also capable of complex information processing. This advance creates new opportunities in neuroscience and neuromorphic engineering, which we discussed at an online focus meeting.

Structural plasticity on an accelerated analog neuromorphic hardware system.

In computational neuroscience, as well as in machine learning, neuromorphic devices promise an accelerated and scalable alternative to neural network simulations. Their neural connectivity and synaptic capacity depend on their specific design choices, but is always intrinsically limited. Here, we present a strategy to achieve structural plasticity that optimizes resource allocation under these constraints by constantly rewiring the pre- and postsynaptic partners while keeping the neuronal fan-in constant and the connectome sparse. In particular, we implemented this algorithm on the analog neuromorphic system BrainScaleS-2. It was executed on a custom embedded digital processor located on chip, accompanying the mixed-signal substrate of spiking neurons and synapse circuits. We evaluated our implementation in a simple supervised learning scenario, showing its ability to optimize the network topology with respect to the nature of its training data, as well as its overall computational efficiency.

Deterministic networks for probabilistic computing.

Neuronal network models of high-level brain functions such as memory recall and reasoning often rely on the presence of some form of noise. The majority of these models assumes that each neuron in the functional network is equipped with its own private source of randomness, often in the form of uncorrelated external noise. In vivo, synaptic background input has been suggested to serve as the main source of noise in biological neuronal networks. However, the finiteness of the number of such noise sources constitutes a challenge to this idea. Here, we show that shared-noise correlations resulting from a finite number of independent noise sources can substantially impair the performance of stochastic network models. We demonstrate that this problem is naturally overcome by replacing the ensemble of independent noise sources by a deterministic recurrent neuronal network. By virtue of inhibitory feedback, such networks can generate small residual spatial correlations in their activity which, counter to intuition, suppress the detrimental effect of shared input. We exploit this mechanism to show that a single recurrent network of a few hundred neurons can serve as a natural noise source for a large ensemble of functional networks performing probabilistic computations, each comprising thousands of units.

Accelerated Physical Emulation of Bayesian Inference in Spiking Neural Networks.

The massively parallel nature of biological information processing plays an important role due to its superiority in comparison to human-engineered computing devices. In particular, it may hold the key to overcoming the von Neumann bottleneck that limits contemporary computer architectures. Physical-model neuromorphic devices seek to replicate not only this inherent parallelism, but also aspects of its microscopic dynamics in analog circuits emulating neurons and synapses. However, these machines require network models that are not only adept at solving particular tasks, but that can also cope with the inherent imperfections of analog substrates. We present a spiking network model that performs Bayesian inference through sampling on the BrainScaleS neuromorphic platform, where we use it for generative and discriminative computations on visual data. By illustrating its functionality on this platform, we implicitly demonstrate its robustness to various substrate-specific distortive effects, as well as its accelerated capability for computation. These results showcase the advantages of brain-inspired physical computation and provide important building blocks for large-scale neuromorphic applications.

Stochasticity from function - Why the Bayesian brain may need no noise.

An increasing body of evidence suggests that the trial-to-trial variability of spiking activity in the brain is not mere noise, but rather the reflection of a sampling-based encoding scheme for probabilistic computing. Since the precise statistical properties of neural activity are important in this context, many models assume an ad-hoc source of well-behaved, explicit noise, either on the input or on the output side of single neuron dynamics, most often assuming an independent Poisson process in either case. However, these assumptions are somewhat problematic: neighboring neurons tend to share receptive fields, rendering both their input and their output correlated; at the same time, neurons are known to behave largely deterministically, as a function of their membrane potential and conductance. We suggest that spiking neural networks may have no need for noise to perform sampling-based Bayesian inference. We study analytically the effect of auto- and cross-correlations in functional Bayesian spiking networks and demonstrate how their effect translates to synaptic interaction strengths, rendering them controllable through synaptic plasticity. This allows even small ensembles of interconnected deterministic spiking networks to simultaneously and co-dependently shape their output activity through learning, enabling them to perform complex Bayesian computation without any need for noise, which we demonstrate in silico, both in classical simulation and in neuromorphic emulation. These results close a gap between the abstract models and the biology of functionally Bayesian spiking networks, effectively reducing the architectural constraints imposed on physical neural substrates required to perform probabilistic computing, be they biological or artificial.

Demonstrating Advantages of Neuromorphic Computation: A Pilot Study.

Neuromorphic devices represent an attempt to mimic aspects of the brain's architecture and dynamics with the aim of replicating its hallmark functional capabilities in terms of computational power, robust learning and energy efficiency. We employ a single-chip prototype of the BrainScaleS 2 neuromorphic system to implement a proof-of-concept demonstration of reward-modulated spike-timing-dependent plasticity in a spiking network that learns to play a simplified version of the Pong video game by smooth pursuit. This system combines an electronic mixed-signal substrate for emulating neuron and synapse dynamics with an embedded digital processor for on-chip learning, which in this work also serves to simulate the virtual environment and learning agent. The analog emulation of neuronal membrane dynamics enables a 1000-fold acceleration with respect to biological real-time, with the entire chip operating on a power budget of 57 mW. Compared to an equivalent simulation using state-of-the-art software, the on-chip emulation is at least one order of magnitude faster and three orders of magnitude more energy-efficient. We demonstrate how on-chip learning can mitigate the effects of fixed-pattern noise, which is unavoidable in analog substrates, while making use of temporal variability for action exploration. Learning compensates imperfections of the physical substrate, as manifested in neuronal parameter variability, by adapting synaptic weights to match respective excitability of individual neurons.

Spiking neurons with short-term synaptic plasticity form superior generative networks.

Spiking networks that perform probabilistic inference have been proposed both as models of cortical computation and as candidates for solving problems in machine learning. However, the evidence for spike-based computation being in any way superior to non-spiking alternatives remains scarce. We propose that short-term synaptic plasticity can provide spiking networks with distinct computational advantages compared to their classical counterparts. When learning from high-dimensional, diverse datasets, deep attractors in the energy landscape often cause mixing problems to the sampling process. Classical algorithms solve this problem by employing various tempering techniques, which are both computationally demanding and require global state updates. We demonstrate how similar results can be achieved in spiking networks endowed with local short-term synaptic plasticity. Additionally, we discuss how these networks can even outperform tempering-based approaches when the training data is imbalanced. We thereby uncover a powerful computational property of the biologically inspired, local, spike-triggered synaptic dynamics based simply on a limited pool of synaptic resources, which enables them to deal with complex sensory data.

Stochastic inference with spiking neurons in the high-conductance state.

The highly variable dynamics of neocortical circuits observed in vivo have been hypothesized to represent a signature of ongoing stochastic inference but stand in apparent contrast to the deterministic response of neurons measured in vitro. Based on a propagation of the membrane autocorrelation across spike bursts, we provide an analytical derivation of the neural activation function that holds for a large parameter space, including the high-conductance state. On this basis, we show how an ensemble of leaky integrate-and-fire neurons with conductance-based synapses embedded in a spiking environment can attain the correct firing statistics for sampling from a well-defined target distribution. For recurrent networks, we examine convergence toward stationarity in computer simulations and demonstrate sample-based Bayesian inference in a mixed graphical model. This points to a new computational role of high-conductance states and establishes a rigorous link between deterministic neuron models and functional stochastic dynamics on the network level.

Probabilistic inference in discrete spaces can be implemented into networks of LIF neurons.

The means by which cortical neural networks are able to efficiently solve inference problems remains an open question in computational neuroscience. Recently, abstract models of Bayesian computation in neural circuits have been proposed, but they lack a mechanistic interpretation at the single-cell level. In this article, we describe a complete theoretical framework for building networks of leaky integrate-and-fire neurons that can sample from arbitrary probability distributions over binary random variables. We test our framework for a model inference task based on a psychophysical phenomenon (the Knill-Kersten optical illusion) and further assess its performance when applied to randomly generated distributions. As the local computations performed by the network strongly depend on the interaction between neurons, we compare several types of couplings mediated by either single synapses or interneuron chains. Due to its robustness to substrate imperfections such as parameter noise and background noise correlations, our model is particularly interesting for implementation on novel, neuro-inspired computing architectures, which can thereby serve as a fast, low-power substrate for solving real-world inference problems.

Characterization and compensation of network-level anomalies in mixed-signal neuromorphic modeling platforms.

Advancing the size and complexity of neural network models leads to an ever increasing demand for computational resources for their simulation. Neuromorphic devices offer a number of advantages over conventional computing architectures, such as high emulation speed or low power consumption, but this usually comes at the price of reduced configurability and precision. In this article, we investigate the consequences of several such factors that are common to neuromorphic devices, more specifically limited hardware resources, limited parameter configurability and parameter variations due to fixed-pattern noise and trial-to-trial variability. Our final aim is to provide an array of methods for coping with such inevitable distortion mechanisms. As a platform for testing our proposed strategies, we use an executable system specification (ESS) of the BrainScaleS neuromorphic system, which has been designed as a universal emulation back-end for neuroscientific modeling. We address the most essential limitations of this device in detail and study their effects on three prototypical benchmark network models within a well-defined, systematic workflow. For each network model, we start by defining quantifiable functionality measures by which we then assess the effects of typical hardware-specific distortion mechanisms, both in idealized software simulations and on the ESS. For those effects that cause unacceptable deviations from the original network dynamics, we suggest generic compensation mechanisms and demonstrate their effectiveness. Both the suggested workflow and the investigated compensation mechanisms are largely back-end independent and do not require additional hardware configurability beyond the one required to emulate the benchmark networks in the first place. We hereby provide a generic methodological environment for configurable neuromorphic devices that are targeted at emulating large-scale, functional neural networks.

Six networks on a universal neuromorphic computing substrate.

In this study, we present a highly configurable neuromorphic computing substrate and use it for emulating several types of neural networks. At the heart of this system lies a mixed-signal chip, with analog implementations of neurons and synapses and digital transmission of action potentials. Major advantages of this emulation device, which has been explicitly designed as a universal neural network emulator, are its inherent parallelism and high acceleration factor compared to conventional computers. Its configurability allows the realization of almost arbitrary network topologies and the use of widely varied neuronal and synaptic parameters. Fixed-pattern noise inherent to analog circuitry is reduced by calibration routines. An integrated development environment allows neuroscientists to operate the device without any prior knowledge of neuromorphic circuit design. As a showcase for the capabilities of the system, we describe the successful emulation of six different neural networks which cover a broad spectrum of both structure and functionality.

A comprehensive workflow for general-purpose neural modeling with highly configurable neuromorphic hardware systems.

In this article, we present a methodological framework that meets novel requirements emerging from upcoming types of accelerated and highly configurable neuromorphic hardware systems. We describe in detail a device with 45 million programmable and dynamic synapses that is currently under development, and we sketch the conceptual challenges that arise from taking this platform into operation. More specifically, we aim at the establishment of this neuromorphic system as a flexible and neuroscientifically valuable modeling tool that can be used by non-hardware experts. We consider various functional aspects to be crucial for this purpose, and we introduce a consistent workflow with detailed descriptions of all involved modules that implement the suggested steps: The integration of the hardware interface into the simulator-independent model description language PyNN; a fully automated translation between the PyNN domain and appropriate hardware configurations; an executable specification of the future neuromorphic system that can be seamlessly integrated into this biology-to-hardware mapping process as a test bench for all software layers and possible hardware design modifications; an evaluation scheme that deploys models from a dedicated benchmark library, compares the results generated by virtual or prototype hardware devices with reference software simulations and analyzes the differences. The integration of these components into one hardware-software workflow provides an ecosystem for ongoing preparative studies that support the hardware design process and represents the basis for the maturity of the model-to-hardware mapping software. The functionality and flexibility of the latter is proven with a variety of experimental results.