Neural circuits consist of many noisy, slow components, with individual neurons subject to ion channel noise, axonal propagation delays, and unreliable and slow synaptic transmission. This raises a fundamental question: how can reliable computation emerge from such unreliable components? A classic strategy is to simply average over a population of
 Award ID(s):
 1845166
 NSFPAR ID:
 10513495
 Editor(s):
 Blohm, Gunnar
 Publisher / Repository:
 PLOS
 Date Published:
 Journal Name:
 PLOS Computational Biology
 Volume:
 18
 Issue:
 10
 ISSN:
 15537358
 Page Range / eLocation ID:
 e1010593
 Format(s):
 Medium: X
 Sponsoring Org:
 National Science Foundation
More Like this

It is widely assumed that distributed neuronal networks are fundamental to the functioning of the brain. Consistent spike timing between neurons is thought to be one of the key principles for the formation of these networks. This can involve synchronous spiking or spiking with time delays, forming spike sequences when the order of spiking is consistent. Finding networks defined by their sequence of timeshifted spikes, denoted here as spike timing networks, is a tremendous challenge. As neurons can participate in multiple spike sequences at multiple betweenspike time delays, the possible complexity of networks is prohibitively large. We present a novel approach that is capable of (1) extracting spike timing networks regardless of their sequence complexity, and (2) that describes their spiking sequences with high temporal precision. We achieve this by decomposing frequencytransformed neuronal spiking into separate networks, characterizing each network’s spike sequence by a time delay per neuron, forming a spike sequence timeline. These networks provide a detailed template for an investigation of the experimental relevance of their spike sequences. Using simulated spike timing networks, we show network extraction is robust to spiking noise, spike timing jitter, and partial occurrences of the involved spike sequences. Using rat multineuron recordings, we demonstrate the approach is capable of revealing real spike timing networks with submillisecond temporal precision. By uncovering spike timing networks, the prevalence, structure, and function of complex spike sequences can be investigated in greater detail, allowing us to gain a better understanding of their role in neuronal functioning.more » « less

null (Ed.)Biological neural networks face a formidable task: performing reliable computations in the face of intrinsic stochasticity in individual neurons, imprecisely specified synaptic connectivity, and nonnegligible delays in synaptic transmission. A common approach to combatting such biological heterogeneity involves averaging over large redundant networks of N neurons resulting in coding errors that decrease classically as the square root of N. Recent work demonstrated a novel mechanism whereby recurrent spiking networks could efficiently encode dynamic stimuli achieving a superclassical scaling in which coding errors decrease as 1/N. This specific mechanism involved two key ideas: predictive coding, and a tight balance, or cancellation between strong feedforward inputs and strong recurrent feedback. However, the theoretical principles governing the efficacy of balanced predictive coding and its robustness to noise, synaptic weight heterogeneity and communication delays remain poorly understood. To discover such principles, we introduce an analytically tractable model of balanced predictive coding, in which the degree of balance and the degree of weight disorder can be dissociated unlike in previous balanced network models, and we develop a meanfield theory of coding accuracy. Overall, our work provides and solves a general theoretical framework for dissecting the differential contributions neural noise, synaptic disorder, chaos, synaptic delays, and balance to the fidelity of predictive neural codes, reveals the fundamental role that balance plays in achieving superclassical scaling, and unifies previously disparate models in theoretical neuroscience.more » « less

Information coding by precise timing of spikes can be faster and more energy efficient than traditional rate coding. However, spiketiming codes are often brittle, which has limited their use in theoretical neuroscience and computing applications. Here, we propose a type of attractor neural network in complex state space and show how it can be leveraged to construct spiking neural networks with robust computational properties through a phasetotiming mapping. Building on Hebbian neural associative memories, like Hopfield networks, we first propose threshold phasor associative memory (TPAM) networks. Complex phasor patterns whose components can assume continuousvalued phase angles and binary magnitudes can be stored and retrieved as stable fixed points in the network dynamics. TPAM achieves high memory capacity when storing sparse phasor patterns, and we derive the energy function that governs its fixedpoint attractor dynamics. Second, we construct 2 spiking neural networks to approximate the complex algebraic computations in TPAM, a reductionist model with resonateandfire neurons and a biologically plausible network of integrateandfire neurons with synaptic delays and recurrently connected inhibitory interneurons. The fixed points of TPAM correspond to stable periodic states of precisely timed spiking activity that are robust to perturbation. The link established between rhythmic firing patterns and complex attractor dynamics has implications for the interpretation of spike patterns seen in neuroscience and can serve as a framework for computation in emerging neuromorphic devices.more » « less

Abstract We study the distribution over measurement outcomes of noisy random quantum circuits in the regime of low fidelity, which corresponds to the setting where the computation experiences at least one gatelevel error with probability close to one. We model noise by adding a pair of weak, unital, singlequbit noise channels after each twoqubit gate, and we show that for typical random circuit instances, correlations between the noisy output distribution
and the corresponding noiseless output distribution$$p_{\text {noisy}}$$ ${p}_{\text{noisy}}$ shrink exponentially with the expected number of gatelevel errors. Specifically, the linear crossentropy benchmark$$p_{\text {ideal}}$$ ${p}_{\text{ideal}}$F that measures this correlation behaves as , where$$F=\text {exp}(2s\epsilon \pm O(s\epsilon ^2))$$ $F=\text{exp}(2s\u03f5\pm O\left(s{\u03f5}^{2}\right))$ is the probability of error per circuit location and$$\epsilon $$ $\u03f5$s is the number of twoqubit gates. Furthermore, if the noise is incoherent—for example, depolarizing or dephasing noise—the total variation distance between the noisy output distribution and the uniform distribution$$p_{\text {noisy}}$$ ${p}_{\text{noisy}}$ decays at precisely the same rate. Consequently, the noisy output distribution can be approximated as$$p_{\text {unif}}$$ ${p}_{\text{unif}}$ . In other words, although at least one local error occurs with probability$$p_{\text {noisy}}\approx Fp_{\text {ideal}}+ (1F)p_{\text {unif}}$$ ${p}_{\text{noisy}}\approx F{p}_{\text{ideal}}+(1F){p}_{\text{unif}}$ , the errors are scrambled by the random quantum circuit and can be treated as global white noise, contributing completely uniform output. Importantly, we upper bound the average total variation error in this approximation by$$1F$$ $1F$ . Thus, the “whitenoise approximation” is meaningful when$$O(F\epsilon \sqrt{s})$$ $O\left(F\u03f5\sqrt{s}\right)$ , a quadratically weaker condition than the$$\epsilon \sqrt{s} \ll 1$$ $\u03f5\sqrt{s}\ll 1$ requirement to maintain high fidelity. The bound applies if the circuit size satisfies$$\epsilon s\ll 1$$ $\u03f5s\ll 1$ , which corresponds to only$$s \ge \Omega (n\log (n))$$ $s\ge \Omega (nlog(n\left)\right)$logarithmic depth circuits, and if, additionally, the inverse error rate satisfies , which is needed to ensure errors are scrambled faster than$$\epsilon ^{1} \ge {\tilde{\Omega }}(n)$$ ${\u03f5}^{1}\ge \stackrel{~}{\Omega}\left(n\right)$F decays. The whitenoise approximation is useful for salvaging the signal from a noisy quantum computation; for example, it was an underlying assumption in complexitytheoretic arguments that noisy random quantum circuits cannot be efficiently sampled classically, even when the fidelity is low. Our method is based on a map from secondmoment quantities in random quantum circuits to expectation values of certain stochastic processes for which we compute upper and lower bounds. 
Biological neural computation is inherently asynchronous due to large variations in neuronal spike timing and transmission delays. Sofar, most theoretical work on neural networks assumes the synchronous setting where neurons fire simultaneously in discrete rounds. In this work we aim at understanding the barriers of asynchronous neural computation from an algorithmic perspective. We consider an extension of the widely studied model of synchronized spiking neurons [Maass, Neural= Networks 97] to the asynchronous setting by taking into account edge and node delays. Edge Delays: We define an asynchronous model for spiking neurons in which the latency values (i.e., transmission delays) of non selfloop edges vary adversarially over time. This extends the recent work of [Hitron and Parter, ESA’19] in which the latency values are restricted to be fixed over time. Our first contribution is an impossibility result that implies that the assumption that selfloop edges have no delays (as assumed in Hitron and Parter) is indeed necessary. Interestingly, in real biological networks selfloop edges (a.k.a. autapse) are indeed free of delays, and the latter has been noted by neuroscientists to be crucial for network synchronization. To capture the computational challenges in this setting, we first consider the implementation of a single NOT gate. This simple function already captures the fundamental difficulties in the asynchronous setting. Our key technical results are space and time upper and lower bounds for the NOT function, our time bounds are tight. In the spirit of the distributed synchronizers [Awerbuch and Peleg, FOCS’90] and following [Hitron and Parter, ESA’19], we then provide a general synchronizer machinery. Our construction is very modular and it is based on efficient circuit implementation of threshold gates. The complexity of our scheme is measured by the overhead in the number of neurons and the computation time, both are shown to be polynomial in the largest latency value, and the largest incoming degree ∆ of the original network. Node Delays: We introduce the study of asynchronous communication due to variations in the response rates of the neurons in the network. In real brain networks, the round duration varies between different neurons in the network. Our key result is a simulation methodology that allows one to transform the above mentioned synchronized solution under edge delays into a synchronized under node delays while incurring a small overhead w.r.t space and time.more » « less