Plasticity Rules Research Articles

Rapid synaptic and gamma rhythm signature of mouse critical period plasticity

Early-life experience enduringly sculpts thalamocortical (TC) axons and sensory processing. Here, we identify the very first synaptic targets that initiate critical period plasticity, heralded by altered cortical oscillations. Monocular deprivation (MD) acutely induced a transient (<3 h) peak in EEG γ-power (~40 Hz) specifically within the visual cortex, but only when the critical period was open (juvenile mice or adults after dark-rearing, Lynx1-deletion, or diazepam-rescued GAD65-deficiency). Rapid TC input loss onto parvalbumin-expressing (PV) inhibitory interneurons (but not onto nearby pyramidal cells) was observed within hours of MD in a TC slice preserving the visual pathway - again once critical periods opened. Computational TC modeling of the emergent γ-rhythm in response to MD delineated a cortical interneuronal gamma (ING) rhythm in networks of PV-cells bearing gap junctions at the start of the critical period. The ING rhythm effectively dissociated thalamic input from cortical spiking, leading to rapid loss of previously strong TC-to-PV connections through standard spike-timing-dependent plasticity rules. As a consequence, previously silent TC-to-PV connections could strengthen on a slower timescale, capturing the gradually increasing γ-frequency and eventual fade-out over time. Thus, ING enables cortical dynamics to transition from being dominated by the strongest TC input to one that senses the statistics of population TC input after MD. Taken together, our findings reveal the initialsynaptic events underlying critical period plasticity and suggest that the fleeting ING accompanying a brief sensory perturbation may serve as a robust readout of TC network state with which to probe developmental trajectories.

Ultra-High Temporal Resolution Visual Reconstruction From a Fovea-Like Spike Camera via Spiking Neuron Model.

Neuromorphic vision sensor is a new bio-inspired imaging paradigm emerged in recent years. It uses the asynchronous spike signals instead of the traditional frame-based manner to achieve ultra-high speed sampling. Unlike the dynamic vision sensor (DVS) that perceives movement by imitating the retinal periphery, the spike camera was developed recently to perceive fine textures by simulating a small retinal region called the fovea. For this new type of neuromorphic camera, how to reconstruct ultra-high speed visual images from spike data becomes an important yet challenging issue in visual scene perception, analysis, and recognition applications. In this paper, a bio-inspired visual reconstruction framework for the spike camera is proposed for the first time. Its core idea is to use the biologically inspired adaptive adjustment mechanisms, combined with the spatiotemporal spike information extracted by the proposed model, to reconstruct the full texture of natural scenes in an ultra-high temporal resolution. Specifically, the proposed model consists of a motion local excitation layer, a spike refining layer and a visual reconstruction layer motivated by the bio-realistic leaky integrate-and-fire (LIF) neurons and synapse connection with spike-timing dependent plasticity (STDP) rule. To evaluate the performance, a spike dataset was constructed for normal and high-speed scenes in real-world recorded by the spike camera. The experimental results show that the proposed approach can reconstruct the visual images with 40,000 frames per second in both normal and high-speed scenes, while achieving high dynamic range and high image quality.

Visuomotor Mismatch Responses as a Hallmark of Explaining Away in Causal Inference.

How are visuomotor mismatch responses in primary visual cortex embedded into cortical processing? We here show that mismatch responses can be understood as the result of a cooperation of motor and visual areas to jointly explain optic flow. This cooperation requires that optic flow is not explained redundantly by both areas, meaning that optic flow inputs to V1 that are predictable from motor neurons should be canceled (i.e., explained away). As a result, neurons in V1 represent only external causes of optic flow, which could allow the animal to easily detect movements that are independent of its own locomotion. We implement the proposed model in a spiking neural network, where coding errors are computed in dendrites and synaptic weights are learned with voltage-dependent plasticity rules. We find that both positive and negative mismatch responses arise, providing an alternative to the prevailing idea that visuomotor mismatch responses are linked to dedicated neurons for error computation. These results also provide a new perspective on several other recent observations of cross-modal neural interactions in cortex.

TMS and neocortical neurons: an integrative review on the micro-macro connection in neuroplasticity.

Tian D, Izumi S. TMS and neocortical neurons: an integrative review on the micro-macro connection in neuroplasticity. Jpn J Compr Rehabil Sci 2023; 14: 1-9. Neuroplasticity plays a pivotal role in neuroscience and neurorehabilitation as it bridges the organization and reorganization properties of the brain. Among the numerous neuroplastic protocols, transcranial magnetic stimulation (TMS) is a well-established non-invasive protocol to induce plastic changes in the brain. Here, we review the findings of four plasticity-inducing TMS protocols in the human motor cortex with relatively evident mechanisms: conventional repetitive TMS (rTMS), theta-burst stimulation (TBS), quadripulse stimulation (QPS) and paired associative stimulation (PAS). Based on the reviewed evidence and a preliminary TMS neurocytological model proposed in our previous report, we further integrate the neurophysiological evidence and plasticity rules of these protocols to present an updated micro-macro connection model between neocortical neurons and the neurophysiological evidence in TMS. This prototypical model will guide further efforts to understand the neural circuit of the motor cortex, the mechanisms of TMS, and the advance of neuroplasticity technologies and their outcomes.

The plasticitome of cortical interneurons.

Hebb postulated that, to store information in the brain, assemblies of excitatory neurons coding for a percept are bound together via associative long-term synaptic plasticity. In this view, it is unclear what role, if any, is carried out by inhibitory interneurons. Indeed, some have argued that inhibitory interneurons are not plastic. Yet numerous recent studies have demonstrated that, similar to excitatory neurons, inhibitory interneurons also undergo long-term plasticity. Here, we discuss the many diverse forms of long-term plasticity that are found at inputs to and outputs from several types of cortical inhibitory interneuron, including their plasticity of intrinsic excitability and their homeostatic plasticity. We explain key plasticity terminology, highlight key interneuron plasticity mechanisms, extract overarching principles and point out implications for healthy brain functionality as well as for neuropathology. We introduce the concept of theplasticitome-the synaptic plasticity counterpart to the genome or the connectome-as well as nomenclature and definitions for dealing with this rich diversity of plasticity. We argue that the great diversity of interneuron plasticity rules is best understood at the circuit level, for example as a way of elucidating how the credit-assignment problem is solved in deep biological neural networks.

Synaptic Characteristic of Hafnia-Based Ferroelectric Tunnel Junction Device for Neuromorphic Computing Application.

Owing to the 4th Industrial Revolution, the amount of unstructured data, such as voice and video data, is rapidly increasing. Brain-inspired neuromorphic computing is a new computing method that can efficiently and parallelly process rapidly increasing data. Among artificial neural networks that mimic the structure of the brain, the spiking neural network (SNN) is a network that imitates the information-processing method of biological neural networks. Recently, memristors have attracted attention as synaptic devices for neuromorphic computing systems. Among them, the ferroelectric doped-HfO2-based ferroelectric tunnel junction (FTJ) is considered as a strong candidate for synaptic devices due to its advantages, such as complementary metal-oxide-semiconductor device/process compatibility, a simple two-terminal structure, and low power consumption. However, research on the spiking operations of FTJ devices for SNN applications is lacking. In this study, the implementation of long-term depression and potentiation as the spike timing-dependent plasticity (STDP) rule in the FTJ device was successful. Based on the measured data, a CrossSim simulator was used to simulate the classification of handwriting images. With a high accuracy of 95.79% for the Mixed National Institute of Standards and Technology (MNIST) dataset, the simulation results demonstrate that our device is capable of differentiating between handwritten images. This suggests that our FTJ device can be used as a synaptic device for implementing an SNN.

Associative memory of structured knowledge

A long standing challenge in biological and artificial intelligence is to understand how new knowledge can be constructed from known building blocks in a way that is amenable for computation by neuronal circuits. Here we focus on the task of storage and recall of structured knowledge in long-term memory. Specifically, we ask how recurrent neuronal networks can store and retrieve multiple knowledge structures. We model each structure as a set of binary relations between events and attributes (attributes may represent e.g., temporal order, spatial location, role in semantic structure), and map each structure to a distributed neuronal activity pattern using a vector symbolic architecture scheme.We then use associative memory plasticity rules to store the binarized patterns as fixed points in a recurrent network. By a combination of signal-to-noise analysis and numerical simulations, we demonstrate that our model allows for efficient storage of these knowledge structures, such that the memorized structures as well as their individual building blocks (e.g., events and attributes) can be subsequently retrieved from partial retrieving cues. We show that long-term memory of structured knowledge relies on a new principle of computation beyond the memory basins. Finally, we show that our model can be extended to store sequences of memories as single attractors.

Sleep-like unsupervised replay reduces catastrophic forgetting in artificial neural networks

Artificial neural networks are known to suffer from catastrophic forgetting: when learning multiple tasks sequentially, they perform well on the most recent task at the expense of previously learned tasks. In the brain, sleep is known to play an important role in incremental learning by replaying recent and old conflicting memory traces. Here we tested the hypothesis that implementing a sleep-like phase in artificial neural networks can protect old memories during new training and alleviate catastrophic forgetting. Sleep was implemented as off-line training with local unsupervised Hebbian plasticity rules and noisy input. In an incremental learning framework, sleep was able to recover old tasks that were otherwise forgotten. Previously learned memories were replayed spontaneously during sleep, forming unique representations for each class of inputs. Representational sparseness and neuronal activity corresponding to the old tasks increased while new task related activity decreased. The study suggests that spontaneous replay simulating sleep-like dynamics can alleviate catastrophic forgetting in artificial neural networks.

Information maximization explains state-dependent synaptic plasticity and memory reorganization during non-rapid eye movement sleep.

Slow waves during the non-rapid eye movement (NREM) sleep reflect the alternating up and down states of cortical neurons; global and local slow waves promote memory consolidation and forgetting, respectively. Furthermore, distinct spike-timing-dependent plasticity (STDP) operates in these up and down states. The contribution of different plasticity rules to neural information coding and memory reorganization remains unknown. Here, we show that optimal synaptic plasticity for information maximization in a cortical neuron model provides a unified explanation for these phenomena. The model indicates that the optimal synaptic plasticity is biased toward depression as the baseline firing rate increases. This property explains the distinct STDP observed in the up and down states. Furthermore, it explains how global and local slow waves predominantly potentiate and depress synapses, respectively, if the background firing rate of excitatory neurons declines with the spatial scale of waves as the model predicts. The model provides a unifying account of the role of NREM sleep, bridging neural information coding, synaptic plasticity, and memory reorganization.

Binary and analog variation of synapses between cortical pyramidal neurons.

Learning from experience depends at least in part on changes in neuronal connections. We present the largest map of connectivity to date between cortical neurons of a defined type (layer 2/3 [L2/3] pyramidal cells in mouse primary visual cortex), which was enabled by automated analysis of serial section electron microscopy images with improved handling of image defects (250 × 140 × 90 μm3 volume). We used the map to identify constraints on the learning algorithms employed by the cortex. Previous cortical studies modeled a continuum of synapse sizes by a log-normal distribution. A continuum is consistent with most neural network models of learning, in which synaptic strength is a continuously graded analog variable. Here, we show that synapse size, when restricted to synapses between L2/3 pyramidal cells, is well modeled by the sum of a binary variable and an analog variable drawn from a log-normal distribution. Two synapses sharing the same presynaptic and postsynaptic cells are known to be correlated in size. We show that the binary variables of the two synapses are highly correlated, while the analog variables are not. Binary variation could be the outcome of a Hebbian or other synaptic plasticity rule depending on activity signals that are relatively uniform across neuronal arbors, while analog variation may be dominated by other influences such as spontaneous dynamical fluctuations. We discuss the implications for the longstanding hypothesis that activity-dependent plasticity switches synapses between bistable states.

H2Learn: High-Efficiency Learning Accelerator for High-Accuracy Spiking Neural Networks

Although spiking neural networks (SNNs) take benefits from the bioplausible neural modeling, the low accuracy under the common local synaptic plasticity learning rules limits their application in many practical tasks. Recently, an emerging SNN supervised learning algorithm inspired by backpropagation through time (BPTT) from the domain of artificial neural networks (ANNs) has successfully boosted the accuracy of SNNs, and helped improve the practicability of SNNs. However, current general-purpose processors suffer from low efficiency when performing BPTT for SNNs due to the ANN-tailored optimization. On the other hand, current neuromorphic chips cannot support BPTT because they mainly adopt local synaptic plasticity rules for simplified implementation. In this work, we propose H2Learn, a novel architecture that can achieve high efficiency for BPTT-based SNN learning, which ensures high accuracy of SNNs. At the beginning, we characterized the behaviors of BPTT-based SNN learning. Benefited from the binary spike-based computation in the forward pass and weight update, we first design look-up table (LUT)-based processing elements in the forward engine and weight update engine to make accumulations implicit and to fuse the computations of multiple input points. Second, benefited from the rich sparsity in the backward pass, we design a dual-sparsity-aware backward engine, which exploits both input and output sparsity. Finally, we apply a pipeline optimization between different engines to build an end-to-end solution for the BPTT-based SNN learning. Compared with the modern NVIDIA V100 GPU, H2Learn achieves <inline-formula xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink"> <tex-math notation="LaTeX">$7.38\times $ </tex-math></inline-formula> area saving, <inline-formula xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink"> <tex-math notation="LaTeX">$5.74-10.20\times $ </tex-math></inline-formula> speedup, and <inline-formula xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink"> <tex-math notation="LaTeX">$5.25-7.12\times $ </tex-math></inline-formula> energy saving on several benchmark datasets.

Brian2CUDA: Flexible and Efficient Simulation of Spiking Neural Network Models on GPUs.

Graphics processing units (GPUs) are widely available and have been used with great success to accelerate scientific computing in the last decade. These advances, however, are often not available to researchers interested in simulating spiking neural networks, but lacking the technical knowledge to write the necessary low-level code. Writing low-level code is not necessary when using the popular Brian simulator, which provides a framework to generate efficient CPU code from high-level model definitions in Python. Here, we present Brian2CUDA, an open-source software that extends the Brian simulator with a GPU backend. Our implementation generates efficient code for the numerical integration of neuronal states and for the propagation of synaptic events on GPUs, making use of their massively parallel arithmetic capabilities. We benchmark the performance improvements of our software for several model types and find that it can accelerate simulations by up to three orders of magnitude compared to Brian's CPU backend. Currently, Brian2CUDA is the only package that supports Brian's full feature set on GPUs, including arbitrary neuron and synapse models, plasticity rules, and heterogeneous delays. When comparing its performance with Brian2GeNN, another GPU-based backend for the Brian simulator with fewer features, we find that Brian2CUDA gives comparable speedups, while being typically slower for small and faster for large networks. By combining the flexibility of the Brian simulator with the simulation speed of GPUs, Brian2CUDA enables researchers to efficiently simulate spiking neural networks with minimal effort and thereby makes the advancements of GPU computing available to a larger audience of neuroscientists.

Voltage-dependent synaptic plasticity: Unsupervised probabilistic Hebbian plasticity rule based on neurons membrane potential

This study proposes voltage-dependent-synaptic plasticity (VDSP), a novel brain-inspired unsupervised local learning rule for the online implementation of Hebb's plasticity mechanism on neuromorphic hardware. The proposed VDSP learning rule updates the synaptic conductance on the spike of the postsynaptic neuron only, which reduces by a factor of two the number of updates with respect to standard spike timing dependent plasticity (STDP). This update is dependent on the membrane potential of the presynaptic neuron, which is readily available as part of neuron implementation and hence does not require additional memory for storage. Moreover, the update is also regularized on synaptic weight and prevents explosion or vanishing of weights on repeated stimulation. Rigorous mathematical analysis is performed to draw an equivalence between VDSP and STDP. To validate the system-level performance of VDSP, we train a single-layer spiking neural network (SNN) for the recognition of handwritten digits. We report 85.01 ± 0.76% (Mean ± SD) accuracy for a network of 100 output neurons on the MNIST dataset. The performance improves when scaling the network size (89.93 ± 0.41% for 400 output neurons, 90.56 ± 0.27 for 500 neurons), which validates the applicability of the proposed learning rule for spatial pattern recognition tasks. Future work will consider more complicated tasks. Interestingly, the learning rule better adapts than STDP to the frequency of input signal and does not require hand-tuning of hyperparameters.

Postsynaptic plasticity of cholinergic synapses underlies the induction and expression of appetitive and familiarity memories in Drosophila.

In vertebrates, several forms of memory-relevant synaptic plasticity involve postsynaptic rearrangements of glutamate receptors. In contrast, previous work indicates that Drosophila and other invertebrates store memories using presynaptic plasticity of cholinergic synapses. Here, we provide evidence for postsynaptic plasticity at cholinergic output synapses from the Drosophila mushroom bodies (MBs). We find that the nicotinic acetylcholine receptor (nAChR) subunit α5 is required within specific MB output neurons for appetitive memory induction but is dispensable for aversive memories. In addition, nAChR α2 subunits mediate memory expression and likely function downstream of α5 and the postsynaptic scaffold protein discs large (Dlg). We show that postsynaptic plasticity traces can be induced independently of the presynapse, and that in vivo dynamics of α2 nAChR subunits are changed both in the context of associative and non-associative (familiarity) memory formation, underlying different plasticity rules. Therefore, regardless of neurotransmitter identity, key principles of postsynaptic plasticity support memory storage across phyla.

Neural representational geometry underlies few-shot concept learning

Understanding the neural basis of the remarkable human cognitive capacity to learn novel concepts from just one or a few sensory experiences constitutes a fundamental problem. We propose a simple, biologically plausible, mathematically tractable, and computationally powerful neural mechanism for few-shot learning of naturalistic concepts. We posit that the concepts that can be learned from few examples are defined by tightly circumscribed manifolds in the neural firing-rate space of higher-order sensory areas. We further posit that a single plastic downstream readout neuron learns to discriminate new concepts based on few examples using a simple plasticity rule. We demonstrate the computational power of our proposal by showing that it can achieve high few-shot learning accuracy on natural visual concepts using both macaque inferotemporal cortex representations and deep neural network (DNN) models of these representations and can even learn novel visual concepts specified only through linguistic descriptors. Moreover, we develop a mathematical theory of few-shot learning that links neurophysiology to predictions about behavioral outcomes by delineating several fundamental and measurable geometric properties of neural representations that can accurately predict the few-shot learning performance of naturalistic concepts across all our numerical simulations. This theory reveals, for instance, that high-dimensional manifolds enhance the ability to learn new concepts from few examples. Intriguingly, we observe striking mismatches between the geometry of manifolds in the primate visual pathway and in trained DNNs. We discuss testable predictions of our theory for psychophysics and neurophysiological experiments.

Paradoxical self-sustained dynamics emerge from orchestrated excitatory and inhibitory homeostatic plasticity rules

Self-sustained neural activity maintained through local recurrent connections is of fundamental importance to cortical function. Converging theoretical and experimental evidence indicates that cortical circuits generating self-sustained dynamics operate in an inhibition-stabilized regime. Theoretical work has established that four sets of weights (WE←E, WE←I, WI←E, and WI←I) must obey specific relationships to produce inhibition-stabilized dynamics, but it is not known how the brain can appropriately set the values of all four weight classes in an unsupervised manner to be in the inhibition-stabilized regime. We prove that standard homeostatic plasticity rules are generally unable to generate inhibition-stabilized dynamics and that their instability is caused by a signature property of inhibition-stabilized networks: the paradoxical effect. In contrast, we show that a family of "cross-homeostatic" rules overcome the paradoxical effect and robustly lead to the emergence of stable dynamics. This work provides a model of how-beginning from a silent network-self-sustained inhibition-stabilized dynamics can emerge from learning rules governing all four synaptic weight classes in an orchestrated manner.

Dual STDP processes at Purkinje cells contribute to distinct improvements in accuracy and speed of saccadic eye movements.

Saccadic eye-movements play a crucial role in visuo-motor control by allowing rapid foveation onto new targets. However, the neural processes governing saccades adaptation are not fully understood. Saccades, due to the short-time of execution (20-100 ms) and the absence of sensory information for online feedback control, must be controlled in a ballistic manner. Incomplete measurements of the movement trajectory, such as the visual endpoint error, are supposedly used to form internal predictions about the movement kinematics resulting in predictive control. In order to characterize the synaptic and neural circuit mechanisms underlying predictive saccadic control, we have reconstructed the saccadic system in a digital controller embedding a spiking neural network of the cerebellum with spike timing-dependent plasticity (STDP) rules driving parallel fiber-Purkinje cell long-term potentiation and depression (LTP and LTD). This model implements a control policy based on a dual plasticity mechanism, resulting in the identification of the roles of LTP and LTD in regulating the overall quality of saccade kinematics: it turns out that LTD increases the accuracy by decreasing visual error and LTP increases the peak speed. The control policy also required cerebellar PCs to be divided into two subpopulations, characterized by burst or pause responses. To our knowledge, this is the first model that explains in mechanistic terms the visual error and peak speed regulation of ballistic eye movements in forward mode exploiting spike-timing to regulate firing in different populations of the neuronal network. This elementary model of saccades could be extended and applied to other more complex cases in which single jerks are concatenated to compose articulated and coordinated movements.

Self-organization of an inhomogeneous memristive hardware for sequence learning

Learning is a fundamental component of creating intelligent machines. Biological intelligence orchestrates synaptic and neuronal learning at multiple time scales to self-organize populations of neurons for solving complex tasks. Inspired by this, we design and experimentally demonstrate an adaptive hardware architecture Memristive Self-organizing Spiking Recurrent Neural Network (MEMSORN). MEMSORN incorporates resistive memory (RRAM) in its synapses and neurons which configure their state based on Hebbian and Homeostatic plasticity respectively. For the first time, we derive these plasticity rules directly from the statistical measurements of our fabricated RRAM-based neurons and synapses. These "technologically plausible” learning rules exploit the intrinsic variability of the devices and improve the accuracy of the network on a sequence learning task by 30%. Finally, we compare the performance of MEMSORN to a fully-randomly-set-up spiking recurrent network on the same task, showing that self-organization improves the accuracy by more than 15%. This work demonstrates the importance of the device-circuit-algorithm co-design approach for implementing brain-inspired computing hardware.

Synaptic Plasticity Is Predicted by Spatiotemporal Firing Rate Patterns and Robust to In Vivo-like Variability.

Synaptic plasticity, the experience-induced change in connections between neurons, underlies learning and memory in the brain. Most of our understanding of synaptic plasticity derives from in vitro experiments with precisely repeated stimulus patterns; however, neurons exhibit significant variability in vivo during repeated experiences. Further, the spatial pattern of synaptic inputs to the dendritic tree influences synaptic plasticity, yet is not considered in most synaptic plasticity rules. Here, we investigate how spatiotemporal synaptic input patterns produce plasticity with in vivo-like conditions using a data-driven computational model with a plasticity rule based on calcium dynamics. Using in vivo spike train recordings as inputs to different size clusters of spines, we show that plasticity is strongly robust to trial-to-trial variability of spike timing. In addition, we derive general synaptic plasticity rules describing how spatiotemporal patterns of synaptic inputs control the magnitude and direction of plasticity. Synapses that strongly potentiated have greater firing rates and calcium concentration later in the trial, whereas strongly depressing synapses have hiring firing rates early in the trial. The neighboring synaptic activity influences the direction and magnitude of synaptic plasticity, with small clusters of spines producing the greatest increase in synaptic strength. Together, our results reveal that calcium dynamics can unify diverse plasticity rules and reveal how spatiotemporal firing rate patterns control synaptic plasticity.

Computational Modeling of Structural Synaptic Plasticity in Echo State Networks.

Most existing studies on computational modeling of neural plasticity have focused on synaptic plasticity. However, regulation of the internal weights in the reservoir based on synaptic plasticity often results in unstable learning dynamics. In this article, a structural synaptic plasticity learning rule is proposed to train the weights and add or remove neurons within the reservoir, which is shown to be able to alleviate the instability of the synaptic plasticity, and to contribute to increase the memory capacity of the network as well. Our experimental results also reveal that a few stronger connections may last for a longer period of time in a constantly changing network structure, and are relatively resistant to decay or disruptions in the learning process. These results are consistent with the evidence observed in biological systems. Finally, we show that an echo state network (ESN) using the proposed structural plasticity rule outperforms an ESN using synaptic plasticity and three state-of-the-art ESNs on four benchmark tasks.