To evaluate the nature of the neural code in the cerebral cortex, we have used a combination of theory and experiment to assess how information is represented in a realistic cortical population response. We have shown how a sensory stimulus could be estimated on a biologically-realistic time scale, given brief individual responses from a population of neurons with similar response properties. For neurons in extrastriate motion area MT, a combinatorial code, one that keeps track of the cell identity of action potentials and silences in individual neurons across the population, carries twice as much information about visual motion as does spike count averaged over the same group of cells. The combinatorial code is more informative because of the diverse firing rate dynamics of MT neurons in response to constant motion stimuli, and is robust to neuron-neuron correlations. We provide a theoretical motivation for these observations that challenges commonly held ideas about the nature of cortical coding at the level of single neurons and neural populations.
We present a model for olfactory coding based on spatial representation of glomerular responses. In this model distinct odorants activate specific subsets of glomeruli, dependent upon the odorant's chemical identity and concentration. The glomerular response specificities are understood statistically, based on experimentally measured distributions of detection thresholds. A simple version of the model, in which glomerular responses are binary (the on/off model), allows us to account quantitatively for the following results of human/rodent olfactory psychophysics: 1) just noticeable differences…
Shannon's seminal 1948 work gave rise to two distinct areas of research: information theory and mathematical coding theory. While information theory has had a strong influence on theoretical neuroscience, ideas from mathematical coding theory have received considerably less attention. Here we take a new look at combinatorial neural codes from a mathematical coding theory perspective, examining the error correction capabilities of familiar receptive field codes (RF codes). We find, perhaps surprisingly, that the high levels of redundancy present in these codes does not support accurate error co…
Correlations among spikes, both on the same neuron and across neurons, are ubiquitous in the brain. For example cross-correlograms can have large peaks, at least in the periphery, and smaller -- but still non-negligible -- ones in cortex, and auto-correlograms almost always exhibit non-trivial temporal structure at a range of timescales. Although this has been known for over forty years, it's still not clear what role these correlations play in the brain -- and, indeed, whether they play any role at all. The goal of this chapter is to shed light on this issue by reviewing some of the work on t…
Neural coding is a key problem in neuroscience, which can promote people's understanding of the mechanism that brain processes information. Among the classical theories of neural coding, the population rate coding has been studied widely in many works. Most computational studies considered the neurons and the corresponding presynaptic synapses as pre-determined excitatory or inhibitory types. According to physiological evidence, however, that the real effect of a synapse is inhibitory or excitatory is determined by the type of the activated receptors. The co-release of excitatory and inhibitor…
The sigmoidal tuning curve that maximizes the mutual information for a Poisson neuron, or population of Poisson neurons, is obtained. The optimal tuning curve is found to have a discrete structure that results in a quantization of the input signal. The number of quantization levels undergoes a hierarchy of phase transitions as the length of the coding window is varied. We postulate, using the mammalian auditory system as an example, that the presence of a subpopulation structure within a neural population is consistent with an optimal neural code.
Neurons in the brain represent information in their collective activity. The fidelity of this neural population code depends on whether and how variability in the response of one neuron is shared with other neurons. Two decades of studies have investigated the influence of these noise correlations on the properties of neural coding. We provide an overview of the theoretical developments on the topic. Using simple, qualitative and general arguments, we discuss, categorize, and relate the various published results. We emphasize the relevance of the fine structure of noise correlation, and we pre…
Most neurons in the primary visual cortex initially respond vigorously when a preferred stimulus is presented, but adapt as stimulation continues. The functional consequences of adaptation are unclear. Typically a reduction of firing rate would reduce single neuron accuracy as less spikes are available for decoding, but it has been suggested that on the population level, adaptation increases coding accuracy. This question requires careful analysis as adaptation not only changes the firing rates of neurons, but also the neural variability and correlations between neurons, which affect coding ac…
Neural encoding plays an important role in faithfully describing the temporally rich patterns, whose instances include human speech and environmental sounds. For tasks that involve classifying such spatio-temporal patterns with the Spiking Neural Networks (SNNs), how these patterns are encoded directly influence the difficulty of the task. In this paper, we compare several existing temporal and population coding schemes and evaluate them on both speech (TIDIGITS) and sound (RWCP) datasets. We show that, with population neural codings, the encoded patterns are linearly separable using the Suppo…
Here, we consider the open issue of how the energy efficiency of neural information transmission process in a general neuronal array constrains the network size, and how well this network size ensures the neural information being transmitted reliably in a noisy environment. By direct mathematical analysis, we have obtained general solutions proving that there exists an optimal neuronal number in the network with which the average coding energy cost (defined as energy consumption divided by mutual information) per neuron passes through a global minimum for both subthreshold and superthreshold s…
A system of globally coupled phase oscillators subject to an external input is considered as a simple model of neural circuits coding external stimulus. The information coding efficiency of the system in its asynchronous state is quantified using Fisher information. The effect of coupling and noise on the information coding efficiency in the stationary state is analyzed. The relaxation process of the system after the presentation of an external input is also studied. It is found that the information coding efficiency exhibits a large transient increase before the system relaxes to the final st…
Previous studies have demonstrated the importance of the primary sensory cortex for the detection, discrimination and awareness of visual stimuli, but it is unknown how neuronal populations in this area process detected and undetected stimuli differently. Critical differences may reside in the mean strength of responses to visual stimuli, as reflected in bulk signals detectable in fMRI, EEG or MEG studies, or may be more subtly composed of differentiated activity of individual sensory neurons. Quantifying single-cell Ca2+ responses to visual stimuli recorded with in vivo 2-photon imaging, we f…
Two prominent strategies that the human visual system uses to reduce incoming information are spatial integration and selective attention. Although spatial integration summarizes and combines information over the visual field, selective attention can single it out for scrutiny. The way in which these well-known mechanisms, with rather opposing effects, interact remains largely unknown. To address this, we had observers perform a gaze-contingent search task that nudged them to deploy either spatial or feature-based attention to maximize performance. We found that, depending on the type of atten…
Which statistical features of spiking activity matter for how stimuli are encoded in neural populations? A vast body of work has explored how firing rates in individual cells and correlations in the spikes of cell pairs impact coding. But little is known about how higher-order correlations, which describe simultaneous firing in triplets and larger ensembles of cells, impact encoded stimulus information. Here, we take a first step toward closing this gap. We vary triplet correlations in small (~10 cell) neural populations while keeping single cell and pairwise statistics fixed at typically repo…
Although Shannon mutual information has been widely used, its effective calculation is often difficult for many practical problems, including those in neural population coding. Asymptotic formulas based on Fisher information sometimes provide accurate approximations to the mutual information but this approach is restricted to continuous variables because the calculation of Fisher information requires derivatives with respect to the encoded variables. In this paper, we consider information-theoretic bounds and approximations of the mutual information based on Kullback--Leibler divergence and Ré…
A general method for deriving maximally informative sigmoidal tuning curves for neural systems with small normalized variability is presented. The optimal tuning curve is a nonlinear function of the cumulative distribution function of the stimulus and depends on the mean-variance relationship of the neural system. The derivation is based on a known relationship between Shannon's mutual information and Fisher information, and the optimality of Jeffrey's prior. It relies on the existence of closed-form solutions to the converse problem of optimizing the stimulus distribution for a given tuning c…
Positive correlations in the activity of neurons are widely observed in the brain. Previous studies have shown these correlations to be detrimental to the fidelity of population codes or at best marginally favorable compared to independent codes. Here, we show that positive correlations can enhance coding performance by astronomical factors. Specifically, the probability of discrimination error can be suppressed by many orders of magnitude. Likewise, the number of stimuli encoded--the capacity--can be enhanced by similarly large factors. These effects do not necessitate unrealistic correlation…
In natural scenes, objects generally appear together with other objects. Yet, theoretical studies of neural population coding typically focus on the encoding of single objects in isolation. Experimental studies suggest that neural responses to multiple objects are well described by linear or nonlinear combinations of the responses to constituent objects, a phenomenon we call stimulus mixing. Here, we present a theoretical analysis of the consequences of common forms of stimulus mixing observed in cortical responses. We show that some of these mixing rules can severely compromise the brain's ab…
Over repeat presentations of the same stimulus, sensory neurons show variable responses. This "noise" is typically correlated between pairs of cells, and a question with rich history in neuroscience is how these noise correlations impact the population's ability to encode the stimulus. Here, we consider a very general setting for population coding, investigating how information varies as a function of noise correlations, with all other aspects of the problem - neural tuning curves, etc. - held fixed. This work yields unifying insights into the role of noise correlations. These are summarized i…
The vicinity of phase transitions selectively amplifies weak stimuli, yielding optimal sensitivity to distinguish external input. Along with this enhanced sensitivity, enhanced levels of fluctuations at criticality reduce the specificity of the response. Given that the specificity of the response is largely compromised when the sensitivity is maximal, the overall benefit of criticality for signal processing remains questionable. Here it is shown that this impasse can be solved by heterogeneous systems incorporating functional diversity, in which critical and subcritical components coexist. The…
We study the reconstruction of visual stimuli from spike trains, recording simultaneously from the two H1 neurons located in the lobula plate of the fly Chrysomya megacephala. The fly views two types of stimuli, corresponding to rotational and translational displacements. If the reconstructed stimulus is to be represented by a Volterra series and correlations between spikes are to be taken into account, first order expansions are insufficient and we have to go to second order, at least. In this case higher order correlation functions have to be manipulated, whose size may become prohibitively …
Motivated by recent studies of population coding in theoretical neuroscience, we examine the optimality of a recently described form of stochastic resonance known as suprathreshold stochastic resonance, which occurs in populations of noisy threshold devices such as models of sensory neurons. Using the mutual information measure, it is shown numerically that for a random input signal, the optimal threshold distribution contains singularities. For large enough noise, this distribution consists of a single point and hence the optimal encoding is realized by the suprathreshold stochastic resonance…
The brain constructs population codes to represent stimuli through widely distributed patterns of activity across neurons. An important figure of merit of population codes is how much information about the original stimulus can be decoded from them. Fisher information is widely used to quantify coding precision and specify optimal codes, because of its relationship to mean squared error (MSE) under certain assumptions. When neural firing is sparse, however, optimizing Fisher information can result in codes that are highly sub-optimal in terms of MSE. We find that this discrepancy arises from t…
The mammalian brain is a metabolically expensive device, and evolutionary pressures have presumably driven it to make productive use of its resources. For sensory areas, this concept has been expressed more formally as an optimality principle: the brain maximizes the information that is encoded about relevant sensory variables, given available resources. Here, we develop this efficiency principle for encoding a sensory variable with a heterogeneous population of noisy neurons, each responding to a particular range of values. The accuracy with which the population represents any particular valu…
Cortical neurons in the fluctuation driven regime can realize ultrafast population encoding. The underlying biophysical mechanisms, however, are not well understood. Reducing the sharpness of the action potential onset can impair ultrafast population encoding, but it is not clear whether a sharp action potential onset is sufficient for ultrafast population encoding. One hypothesis proposes that the sharp action potential onset is caused by the electrotonic separation of the site of action potential initiation from the soma, and that this spatial separation also results in ultrafast population …
Following a stimulus, the neural response typically strongly varies in time and across neurons before settling to a steady-state. While classical population coding theory disregards the temporal dimension, recent works have argued that trajectories of transient activity can be particularly informative about stimulus identity and may form the basis of computations through dynamics. Yet the dynamical mechanisms needed to generate a population code based on transient trajectories have not been fully elucidated. Here we examine transient coding in a broad class of high-dimensional linear networks …
Efficient coding under constraint drives neural systems towards criticality and sloppiness
Institute of Theoretical Physics, Chinese Academy of Sciences（中国科学院理论物理研究所）；School of Physical Sciences, University of Chinese Academy of Sciences（中国科学院大学物理科学学院）
Neurons in the nervous system convey information to higher brain regions by the generation of spike trains. An important question in the field of computational neuroscience is how these sensory neurons encode environmental information in a way which may be simply analyzed by subsequent systems. Many aspects of the form and function of the nervous system have been understood using the concepts of optimal population coding. Most studies, however, have neglected the aspect of temporal coding. Here we address this shortcoming through a filtering theory of inhomogeneous Poisson processes. We derive…
Norwegian University of Science and Technology（挪威科技大学）；Bosch Center for Artificial Intelligence（博世人工智能中心）；University of Cambridge（剑桥大学）
Systems neuroscience relies on two complementary views of neural data, characterized by single neuron tuning curves and analysis of population activity. These two perspectives combine elegantly in neural latent variable models that constrain the relationship between latent variables and neural activity, modeled by simple tuning curve functions. This has recently been demonstrated using Gaussian processes, with applications to realistic and topologically relevant latent manifolds. Those and previous models, however, missed crucial shared coding properties of neural populations. We propose featu…
The coding mechanism of sensory memory on the neuron scale is one of the most important questions in neuroscience. We have put forward a quantitative neural network model, which is self organized, self similar, and self adaptive, just like an ecosystem following Darwin theory. According to this model, neural coding is a mult to one mapping from objects to neurons. And the whole cerebrum is a real-time statistical Turing Machine, with powerful representing and learning ability. This model can reconcile some important disputations, such as: temporal coding versus rate based coding, grandmother c…
Quian Quiroga et al. [Nature 435, 1102 (2005)] have recently discovered neurons that appear to have the characteristics of grandmother (GM) cells. Here we quantitatively assess the compatibility of their data with the GM-cell hypothesis. We show that, contrary to the general impression, a GM-cell representation can be information-theoretically efficient, but that it must be accompanied by cells giving a distributed coding of the input. We present a general method to deduce the sparsity distribution of the whole neuronal population from a sample, and use it to show there are two populations of …
In neuroscience, population coding theory demonstrates that neural assemblies can achieve fault-tolerant information processing. Mapped to nanoelectronics, this strategy could allow for reliable computing with scaled-down, noisy, imperfect devices. Doing so requires that the population components form a set of basis functions in terms of their response functions to inputs, offering a physical substrate for calculating. For this purpose, the responses of the nanodevices should be non-linear, and each tuned to different values of the input. These strong requirements have prevented a demonstratio…
The manner in which groups of neurons represent events in the external world is fundamental to neuroscience. Here, we analyze the population code of the retina during naturalistic stimulation and show that the information conveyed by specific multi-neuronal firing patterns can be very different from the sum of the pattern's parts. Synchronous spikes convey more information than either of the participating cells, but almost always less than their sum, making them redundant coding symbols. Surprisingly, patterns of spiking and silence are mostly synergistic - carrying information that is accessi…
Insects identify and evaluate behaviorally relevant odorants in complex natural scenes where odor concentrations and mixture composition can change rapidly. In the honeybee, a combinatorial code of activated and inactivated projection neurons (PNs) develops rapidly within tens of milliseconds at the first level of neural integration, the antennal lobe (AL). The phasic-tonic stimulus-response dynamics observed in the neural population code and in the firing rate profiles of single neurons is faithfully captured by two alternative models which rely either on short-term synaptic depression, or on…
While recent recordings from neural populations show beyond-pairwise, or higher-order correlations (HOC), we have little understanding of how HOC arise from network interactions and of how they impact encoded information. Here, we show that input nonlinearities imply HOC in spin-glass-type statistical models. We then discuss one such model with parameterized pairwise- and higher-order interactions, revealing conditions under which beyond-pairwise interactions increase the mutual information between a given stimulus type and the population responses. For jointly Gaussian stimuli, coding perform…
In this work we explore encoding strategies learned by statistical models of sensory coding in noisy spiking networks. Early stages of sensory communication in neural systems can be viewed as encoding channels in the information-theoretic sense. However, neural populations face constraints not commonly considered in communications theory. Using restricted Boltzmann machines as a model of sensory encoding, we find that networks with sufficient capacity learn to balance precision and noise-robustness in order to adaptively communicate stimuli with varying information content. Mirroring variabili…
The generation and conduction of action potentials represents a fundamental means of communication in the nervous system, and is a metabolically expensive process. In this paper, we investigate the energy efficiency of neural systems in a process of transfer pulse signals with action potentials. By computer simulation of a stochastic version of Hodgkin-Huxley model with detailed description of ion channel random gating, and analytically solve a bistable neuron model that mimic the action potential generation with a particle crossing the barrier of a double well, we find optimal number of ion c…
Background: Spike trains of multiple neurons can be analyzed following the summed population (SP) or the labeled line (LL) hypothesis. Responses to external stimuli are generated by a neuronal population as a whole or the individual neurons have encoding capacities of their own. The SPIKE-distance estimated either for a single, pooled spike train over a population or for each neuron separately can serve to quantify these responses. New Method: For the SP case we compare three algorithms that search for the most discriminative subpopulation over all stimulus pairs. For the LL case we introduce …
In this study, we analyzed the activity of monkey V1 neurons responding to grating stimuli of different orientations using inference methods for a time-dependent Ising model. The method provides optimal estimation of time-dependent neural interactions with credible intervals according to the sequential Bayes estimation algorithm. Furthermore, it allows us to trace dynamics of macroscopic network properties such as entropy, sparseness, and fluctuation. Here we report that, in all examined stimulus conditions, pairwise interactions contribute to increasing sparseness and fluctuation. We then dem…
