Early selection of task-relevant features through population gating.

Brains can gracefully weed out irrelevant stimuli to guide behavior. This feat is believed to rely on a progressive selection of task-relevant stimuli across the cortical hierarchy, but the specific across-area interactions enabling stimulus selection are still unclear. Here, we propose that population gating, occurring within primary auditory cortex (A1) but controlled by top-down inputs from prelimbic region of medial prefrontal cortex (mPFC), can support across-area stimulus selection. Examining single-unit activity recorded while rats performed an auditory context-dependent task, we found that A1 encoded relevant and irrelevant stimuli along a common dimension of its neural space. Yet, the relevant stimulus encoding was enhanced along an extra dimension. In turn, mPFC encoded only the stimulus relevant to the ongoing context. To identify candidate mechanisms for stimulus selection within A1, we reverse-engineered low-rank RNNs trained on a similar task. Our analyses predicted that two context-modulated neural populations gated their preferred stimulus in opposite contexts, which we confirmed in further analyses of A1. Finally, we show in a two-region RNN how population gating within A1 could be controlled by top-down inputs from PFC, enabling flexible across-area communication despite fixed inter-areal connectivity.

Limited-control optimal protocols arbitrarily far from equilibrium.

Recent studies have explored finite-time dissipation-minimizing protocols for stochastic thermodynamic systems driven arbitrarily far from equilibrium, when granted full external control to drive the system. However, in both simulation and experimental contexts, systems often may only be controlled with a limited set of degrees of freedom. Here, going beyond slow- and fast-driving approximations employed in previous studies, we obtain exact finite-time optimal protocols for this limited-control setting. By working with deterministic Fokker-Planck probability density time evolution, we can frame the work-minimizing protocol problem in the standard form of an optimal control theory problem. We demonstrate that finding the exact optimal protocol is equivalent to solving a system of Hamiltonian partial differential equations, which in many cases admit efficiently calculable numerical solutions. Within this framework, we reproduce analytical results for the optimal control of harmonic potentials and numerically devise optimal protocols for two anharmonic examples: varying the stiffness of a quartic potential and linearly biasing a double-well potential. We confirm that these optimal protocols outperform other protocols produced through previous methods, in some cases by a substantial amount. We find that for the linearly biased double-well problem, the mean position under the optimal protocol travels at a near-constant velocity. Surprisingly, for a certain timescale and barrier height regime, the optimal protocol is also nonmonotonic in time.

Optimal finite-time Brownian Carnot engine.

Recent advances in experimental control of colloidal systems have spurred a revolution in the production of mesoscale thermodynamic devices. Functional "textbook" engines, such as the Stirling and Carnot cycles, have been produced in colloidal systems where they operate far from equilibrium. Simultaneously, significant theoretical advances have been made in the design and analysis of such devices. Here, we use methods from thermodynamic geometry to characterize the optimal finite-time nonequilibrium cyclic operation of the parametric harmonic oscillator in contact with a time-varying heat bath with particular focus on the Brownian Carnot cycle. We derive the optimally parametrized Carnot cycle, along with two other new cycles and compare their dissipated energy, efficiency, and steady-state power production against each other and a previously tested experimental protocol for the Carnot cycle. We demonstrate a 20% improvement in dissipated energy over previous experimentally tested protocols and a ∼50% improvement under other conditions for one of our engines, whereas our final engine is more efficient and powerful than the others we considered. Our results provide the means for experimentally realizing optimal mesoscale heat engines.

Geometric Bound on the Efficiency of Irreversible Thermodynamic Cycles.

Stochastic thermodynamics has revolutionized our understanding of heat engines operating in finite time. Recently, numerous studies have considered the optimal operation of thermodynamic cycles acting as heat engines with a given profile in thermodynamic space (e.g., P-V space in classical thermodynamics), with a particular focus on the Carnot engine. In this work, we use the lens of thermodynamic geometry to explore the full space of thermodynamic cycles with continuously varying bath temperature in search of optimally shaped cycles acting in the slow-driving regime. We apply classical isoperimetric inequalities to derive a universal geometric bound on the efficiency of any irreversible thermodynamic cycle and explicitly construct efficient heat engines operating in finite time that nearly saturate this bound for a specific model system. Given the bound, these optimal cycles perform more efficiently than all other thermodynamic cycles operating as heat engines in finite time, including notable cycles, such as those of Carnot, Stirling, and Otto. For example, in comparison to recent experiments, this corresponds to orders of magnitude improvement in the efficiency of engines operating in certain time regimes. Our results suggest novel design principles for future mesoscopic heat engines and are ripe for experimental investigation.

Solution to the Fokker-Planck equation for slowly driven Brownian motion: Emergent geometry and a formula for the corresponding thermodynamic metric.

Considerable progress has recently been made with geometrical approaches to understanding and controlling small out-of-equilibrium systems, but a mathematically rigorous foundation for these methods has been lacking. Towards this end, we develop a perturbative solution to the Fokker-Planck equation for one-dimensional driven Brownian motion in the overdamped limit enabled by the spectral properties of the corresponding single-particle Schrödinger operator. The perturbation theory is in powers of the inverse characteristic timescale of variation of the fastest varying control parameter, measured in units of the system timescale, which is set by the smallest eigenvalue of the corresponding Schrödinger operator. It applies to any Brownian system for which the Schrödinger operator has a confining potential. We use the theory to rigorously derive an exact formula for a Riemannian "thermodynamic" metric in the space of control parameters of the system. We show that up to second-order terms in the perturbation theory, optimal dissipation-minimizing driving protocols minimize the length defined by this metric. We also show that a previously proposed metric is calculable from our exact formula with corrections that are exponentially suppressed in a characteristic length scale. We illustrate our formula using the two-dimensional example of a harmonic oscillator with time-dependent spring constant in a time-dependent electric field. Lastly, we demonstrate that the Riemannian geometric structure of the optimal control problem is emergent; it derives from the form of the perturbative expansion for the probability density and persists to all orders of the expansion.

Critical Point-Finding Methods Reveal Gradient-Flat Regions of Deep Network Losses.

Despite the fact that the loss functions of deep neural networks are highly nonconvex, gradient-based optimization algorithms converge to approximately the same performance from many random initial points. One thread of work has focused on explaining this phenomenon by numerically characterizing the local curvature near critical points of the loss function, where the gradients are near zero. Such studies have reported that neural network losses enjoy a no-bad-local-minima property, in disagreement with more recent theoretical results. We report here that the methods used to find these putative critical points suffer from a bad local minima problem of their own: they often converge to or pass through regions where the gradient norm has a stationary point. We call these gradient-flat regions, since they arise when the gradient is approximately in the kernel of the Hessian, such that the loss is locally approximately linear, or flat, in the direction of the gradient. We describe how the presence of these regions necessitates care in both interpreting past results that claimed to find critical points of neural network losses and in designing second-order methods for optimizing neural networks.

Engineered swift equilibration for arbitrary geometries.

Engineered swift equilibration (ESE) is a class of driving protocols that enforce an equilibrium distribution with respect to external control parameters at the beginning and end of rapid state transformations of open, classical nonequilibrium systems. ESE protocols have previously been derived and experimentally realized for Brownian particles in simple, one-dimensional, time-varying trapping potentials; one recent study considered ESE in two-dimensional Euclidean configuration space. Here we extend the ESE framework to generic, overdamped Brownian systems in arbitrary curved configuration space and illustrate our results with specific examples not amenable to previous techniques. Our approach may be used to impose the necessary dynamics to control the full temporal configurational distribution in a wide variety of experimentally realizable settings.

Efficient sensory coding of multidimensional stimuli.

According to the efficient coding hypothesis, sensory systems are adapted to maximize their ability to encode information about the environment. Sensory neurons play a key role in encoding by selectively modulating their firing rate for a subset of all possible stimuli. This pattern of modulation is often summarized via a tuning curve. The optimally efficient distribution of tuning curves has been calculated in variety of ways for one-dimensional (1-D) stimuli. However, many sensory neurons encode multiple stimulus dimensions simultaneously. It remains unclear how applicable existing models of 1-D tuning curves are for neurons tuned across multiple dimensions. We describe a mathematical generalization that builds on prior work in 1-D to predict optimally efficient multidimensional tuning curves. Our results have implications for interpreting observed properties of neuronal populations. For example, our results suggest that not all tuning curve attributes (such as gain and bandwidth) are equally useful for evaluating the encoding efficiency of a population.

Heterogeneous Synaptic Weighting Improves Neural Coding in the Presence of Common Noise.

Simultaneous recordings from the cortex have revealed that neural activity is highly variable and that some variability is shared across neurons in a population. Further experimental work has demonstrated that the shared component of a neuronal population's variability is typically comparable to or larger than its private component. Meanwhile, an abundance of theoretical work has assessed the impact that shared variability has on a population code. For example, shared input noise is understood to have a detrimental impact on a neural population's coding fidelity. However, other contributions to variability, such as common noise, can also play a role in shaping correlated variability. We present a network of linear-nonlinear neurons in which we introduce a common noise input to model-for instance, variability resulting from upstream action potentials that are irrelevant to the task at hand. We show that by applying a heterogeneous set of synaptic weights to the neural inputs carrying the common noise, the network can improve its coding ability as measured by both Fisher information and Shannon mutual information, even in cases where this results in amplification of the common noise. With a broad and heterogeneous distribution of synaptic weights, a population of neurons can remove the harmful effects imposed by afferents that are uninformative about a stimulus. We demonstrate that some nonlinear networks benefit from weight diversification up to a certain population size, above which the drawbacks from amplified noise dominate over the benefits of diversification. We further characterize these benefits in terms of the relative strength of shared and private variability sources. Finally, we studied the asymptotic behavior of the mutual information and Fisher information analytically in our various networks as a function of population size. We find some surprising qualitative changes in the asymptotic behavior as we make seemingly minor changes in the synaptic weight distributions.

Replay as wavefronts and theta sequences as bump oscillations in a grid cell attractor network.

Grid cells fire in sequences that represent rapid trajectories in space. During locomotion, theta sequences encode sweeps in position starting slightly behind the animal and ending ahead of it. During quiescence and slow wave sleep, bouts of synchronized activity represent long trajectories called replays, which are well-established in place cells and have been recently reported in grid cells. Theta sequences and replay are hypothesized to facilitate many cognitive functions, but their underlying mechanisms are unknown. One mechanism proposed for grid cell formation is the continuous attractor network. We demonstrate that this established architecture naturally produces theta sequences and replay as distinct consequences of modulating external input. Driving inhibitory interneurons at the theta frequency causes attractor bumps to oscillate in speed and size, which gives rise to theta sequences and phase precession, respectively. Decreasing input drive to all neurons produces traveling wavefronts of activity that are decoded as replays.

Design of optical neural networks with component imprecisions.

For the benefit of designing scalable, fault resistant optical neural networks (ONNs), we investigate the effects architectural designs have on the ONNs' robustness to imprecise components. We train two ONNs - one with a more tunable design (GridNet) and one with better fault tolerance (FFTNet) - to classify handwritten digits. When simulated without any imperfections, GridNet yields a better accuracy (∼98%) than FFTNet (∼95%). However, under a small amount of error in their photonic components, the more fault tolerant FFTNet overtakes GridNet. We further provide thorough quantitative and qualitative analyses of ONNs' sensitivity to varying levels and types of imprecisions. Our results offer guidelines for the principled design of fault-tolerant ONNs as well as a foundation for further research.

Spike-timing-dependent ensemble encoding by non-classically responsive cortical neurons.

Neurons recorded in behaving animals often do not discernibly respond to sensory input and are not overtly task-modulated. These non-classically responsive neurons are difficult to interpret and are typically neglected from analysis, confounding attempts to connect neural activity to perception and behavior. Here, we describe a trial-by-trial, spike-timing-based algorithm to reveal the coding capacities of these neurons in auditory and frontal cortex of behaving rats. Classically responsive and non-classically responsive cells contained significant information about sensory stimuli and behavioral decisions. Stimulus category was more accurately represented in frontal cortex than auditory cortex, via ensembles of non-classically responsive cells coordinating the behavioral meaning of spike timings on correct but not error trials. This unbiased approach allows the contribution of all recorded neurons - particularly those without obvious task-related, trial-averaged firing rate modulation - to be assessed for behavioral relevance on single trials.

Minimum and Maximum Entropy Distributions for Binary Systems with Known Means and Pairwise Correlations.

Maximum entropy models are increasingly being used to describe the collective activity of neural populations with measured mean neural activities and pairwise correlations, but the full space of probability distributions consistent with these constraints has not been explored. We provide upper and lower bounds on the entropy for the minimum entropy distribution over arbitrarily large collections of binary units with any fixed set of mean values and pairwise correlations. We also construct specific low-entropy distributions for several relevant cases. Surprisingly, the minimum entropy solution has entropy scaling logarithmically with system size for any set of first- and second-order statistics consistent with arbitrarily large systems. We further demonstrate that some sets of these low-order statistics can only be realized by small systems. Our results show how only small amounts of randomness are needed to mimic low-order statistical properties of highly entropic distributions, and we discuss some applications for engineered and biological information transmission systems.

Entropy Production and Fluctuation Theorems for Active Matter.

Active biological systems reside far from equilibrium, dissipating heat even in their steady state, thus requiring an extension of conventional equilibrium thermodynamics and statistical mechanics. In this Letter, we have extended the emerging framework of stochastic thermodynamics to active matter. In particular, for the active Ornstein-Uhlenbeck model, we have provided consistent definitions of thermodynamic quantities such as work, energy, heat, entropy, and entropy production at the level of single, stochastic trajectories and derived related fluctuation relations. We have developed a generalization of the Clausius inequality, which is valid even in the presence of the non-Hamiltonian dynamics underlying active matter systems. We have illustrated our results with explicit numerical studies.

Nonequilibrium work energy relation for non-Hamiltonian dynamics.

Recent years have witnessed major advances in our understanding of nonequilibrium processes. The Jarzynski equality, for example, provides a link between equilibrium free energy differences and finite-time nonequilibrium dynamics. We propose a generalization of this relation to non-Hamiltonian dynamics, relevant for active matter systems, continuous feedback, and computer simulation. Surprisingly, this relation allows us to calculate the free energy difference between the desired initial and final equilibrium states using arbitrary dynamics. As a practical matter, this dissociation between the dynamics and the initial and final states promises to facilitate a range of techniques for free energy estimation in a single universal expression.

Optimal protocols for slowly driven quantum systems.

The design of efficient quantum information processing will rely on optimal nonequilibrium transitions of driven quantum systems. Building on a recently developed geometric framework for computing optimal protocols for classical systems driven in finite time, we construct a general framework for optimizing the average information entropy for driven quantum systems. Geodesics on the parameter manifold endowed with a positive semidefinite metric correspond to protocols that minimize the average information entropy production in finite time. We use this framework to explicitly compute the optimal entropy production for a simple two-state quantum system coupled to a heat bath of bosonic oscillators, which has applications to quantum annealing.

Optimal control of overdamped systems.

Nonequilibrium physics encompasses a broad range of natural and synthetic small-scale systems. Optimizing transitions of such systems will be crucial for the development of nanoscale technologies and may reveal the physical principles underlying biological processes at the molecular level. Recent work has demonstrated that when a thermodynamic system is driven away from equilibrium then the space of controllable parameters has a Riemannian geometry induced by a generalized inverse diffusion tensor. We derive a simple, compact expression for the inverse diffusion tensor that depends solely on equilibrium information for a broad class of potentials. We use this formula to compute the minimal dissipation for two model systems relevant to small-scale information processing and biological molecular motors. In the first model, we optimally erase a single classical bit of information modeled by an overdamped particle in a smooth double-well potential. In the second model, we find the minimal dissipation of a simple molecular motor model coupled to an optical trap. In both models, we find that the minimal dissipation for the optimal protocol of duration τ is proportional to 1/τ, as expected, though the dissipation for the erasure model takes a different form than what we found previously for a similar system.

Time resolution dependence of information measures for spiking neurons: scaling and universality.

The mutual information between stimulus and spike-train response is commonly used to monitor neural coding efficiency, but neuronal computation broadly conceived requires more refined and targeted information measures of input-output joint processes. A first step toward that larger goal is to develop information measures for individual output processes, including information generation (entropy rate), stored information (statistical complexity), predictable information (excess entropy), and active information accumulation (bound information rate). We calculate these for spike trains generated by a variety of noise-driven integrate-and-fire neurons as a function of time resolution and for alternating renewal processes. We show that their time-resolution dependence reveals coarse-grained structural properties of interspike interval statistics; e.g., τ-entropy rates that diverge less quickly than the firing rate indicated by interspike interval correlations. We also find evidence that the excess entropy and regularized statistical complexity of different types of integrate-and-fire neurons are universal in the continuous-time limit in the sense that they do not depend on mechanism details. This suggests a surprising simplicity in the spike trains generated by these model neurons. Interestingly, neurons with gamma-distributed ISIs and neurons whose spike trains are alternating renewal processes do not fall into the same universality class. These results lead to two conclusions. First, the dependence of information measures on time resolution reveals mechanistic details about spike train generation. Second, information measures can be used as model selection tools for analyzing spike train processes.

Rats Exert Executive Control.

In this issue of Neuron, Duan et al. (2015) introduce a novel rodent model of executive control. Their neural recordings provide direct evidence for the task-set inertia theory and suggest a crucial role for the superior colliculus in executive control.