Neurons in the nervous system exhibit an outstanding variety of morphological and physiological properties. However, close to threshold, this remarkable richness may be grouped succinctly into two basic types of excitability, often referred to as type I and type II. The dynamical traits of these two neuron types have been extensively characterized. It would be interesting, however, to understand the information-processing consequences of their dynamical properties. To that end, here we determine the differences between the stimulus features inducing firing in type I and in type II neurons. We work both with realistic conductance-based models and minimal normal forms. We conclude that type I neurons fire in response to scale-free depolarizing stimuli. Type II neurons, instead, are most efficiently driven by input stimuli containing both depolarizing and hyperpolarizing phases, with significant power in the frequency band corresponding to the intrinsic frequencies of the cell.
The effect of environmental temperature on neuronal spiking behaviors is investigated by numerically simulating the temperature dependence of spiking threshold of the Hodgkin-Huxley neuron subject to synaptic stimulus. We find that the spiking threshold exhibits a global minimum in a "comfortable temperature" range where spike initiation needs weakest synaptic strength, indicating the occurrence of optimal use of synaptic transmission in neural system. We further explore the biophysical origin of this phenomenon in ion channel gating kinetics and also discuss its possible biological relevance …
When two stimuli are present in the receptive field of a V4 neuron, the firing rate response is between the weakest and strongest response elicited by each of the stimuli alone (Reynolds et al, 1999, Journal of Neuroscience 19:1736-1753). When attention is directed towards the stimulus eliciting the strongest response (the preferred stimulus), the response to the pair is increased, whereas the response decreases when attention is directed to the other stimulus (the poor stimulus). These experimental results were reproduced in a model of a V4 neuron under the assumption that attention modulates…
We consider a threshold-crossing spiking process as a simple model for the activity within a population of neurons. Assuming that these neurons are driven by a common fluctuating input with Gaussian statistics, we evaluate the cross-correlation of spike trains in pairs of model neurons with different thresholds. This correlation function tends to be asymmetric in time, indicating a preference for the neuron with the lower threshold to fire before the one with the higher threshold, even if their inputs are identical. The relationship between these results and spike statistics in other models of…
Neurons in the primate visual cortices show a wide range of stimulus selectivity. Some neurons respond to only a small fraction of stimulus images, whereas others respond to many stimulus images in a non-selective manner. It is unclear how stimulus selective and non-selective neurons contribute to visual object recognition. Herein, we examined the relationship between stimulus selectivity and the effect of deletion of units on task performance using fully a connected layer of two types of deep convolutional neural networks (DCNNs). Deleting a stimulus selective unit caused slight improvements …
The coding properties of cells with different types of receptive fields have been studied for decades. ON-type neurons fire in response to positive fluctuations of the time-dependent stimulus, whereas OFF cells are driven by negative stimulus segments. Biphasic cells, in turn, are selective to up/down or down/up stimulus upstrokes. In this paper, we explore the way in which different receptive fields affect the firing statistics of Poisson neuron models, when driven with slow stimuli. We find analytical expressions for the time-dependent peri-stimulus time histogram and the inter-spike interva…
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 …
We present a theoretical study aiming at model fitting for sensory neurons. Conventional neural network training approaches are not applicable to this problem due to lack of continuous data. Although the stimulus can be considered as a smooth time dependent variable, the associated response will be a set of neural spike timings (roughly the instants of successive action potential peaks) which have no amplitude information. A recurrent neural network model can be fitted to such a stimulus-response data pair by using maximum likelihood estimation method where the likelihood function is derived f…
To compensate for sensory processing delays, the visual system must make predictions to ensure timely and appropriate behaviors. Recent work has found predictive information about the stimulus in neural populations early in vision processing, starting in the retina. However, to utilize this information, cells downstream must in turn be able to read out the predictive information from the spiking activity of retinal ganglion cells. Here we investigate whether a downstream cell could learn efficient encoding of predictive information in its inputs in the absence of other instructive signals, fro…
Neural oscillations are universal phenomena and can be observed at different levels of neural systems, from single neuron to macroscopic brain. The frequency of those oscillations are related to the brain functions. However, little is know about how the oscillating frequency of neural system affects neural information transmission in them. In this paper, we investigated how the signal processing in single neuron is modulated by subthreshold membrane potential oscillation generated by upstream rhythmic neural activities. We found that the high frequency oscillations facilitate the transferring …
Neurons in cortical circuits exhibit coordinated spiking activity, and can produce correlated synchronous spikes during behavior and cognition. We recently developed a method for estimating the dynamics of correlated ensemble activity by combining a model of simultaneous neuronal interactions (e.g., a spin-glass model) with a state-space method (Shimazaki et al. 2012 PLoS Comput Biol 8 e1002385). This method allows us to estimate stimulus-evoked dynamics of neuronal interactions which is reproducible in repeated trials under identical experimental conditions. However, the method may not be sui…
Correlations in sensory neural networks have both extrinsic and intrinsic origins. Extrinsic or stimulus correlations arise from shared inputs to the network, and thus depend strongly on the stimulus ensemble. Intrinsic or noise correlations reflect biophysical mechanisms of interactions between neurons, which are expected to be robust to changes of the stimulus ensemble. Despite the importance of this distinction for understanding how sensory networks encode information collectively, no method exists to reliably separate intrinsic interactions from extrinsic correlations in neural activity da…
The ability of the organism to distinguish between various stimuli is limited by the structure and noise in the population code of its sensory neurons. Here we infer a distance measure on the stimulus space directly from the recorded activity of 100 neurons in the salamander retina. In contrast to previously used measures of stimulus similarity, this "neural metric" tells us how distinguishable a pair of stimulus clips is to the retina, given the noise in the neural population response. We show that the retinal distance strongly deviates from Euclidean, or any static metric, yet has a simple s…
Several studies have shown that bursting neurons can encode information in the number of spikes per burst: As the stimulus varies, so does the length of individual bursts. The represented stimuli, however, vary substantially among different sensory modalities and different neurons. The goal of this paper is to determine which kind of stimulus features can be encoded in burst length, and how those features depend on the mathematical properties of the underlying dynamical system. We show that the initiation and termination of each burst is triggered by specific stimulus features whose temporal c…
The functional relationship between an input and a sensory neuron's response can be described by the neuron's stimulus-response mapping function. A general approach for characterizing the stimulus-response mapping function is called system identification. Many different names have been used for the stimulus-response mapping function: kernel or transfer function, transducer, spatiotemporal receptive field. Many algorithms have been developed to estimate a neuron's mapping function from an ensemble of stimulus-response pairs. These include the spike-triggered average, normalized reverse correlat…
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…
Neural coding is a field of study that concerns how sensory information is represented in the brain by networks of neurons. The link between external stimulus and neural response can be studied from two parallel points of view. The first, neural encoding refers to the mapping from stimulus to response, and primarily focuses on understanding how neurons respond to a wide variety of stimuli, and on constructing models that accurately describe the stimulus-response relationship. Neural decoding, on the other hand, refers to the reverse mapping, from response to stimulus, where the challenge is to…
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…
We show that dynamical gain modulation of neurons' stimulus response is described as an information-theoretic cycle that generates entropy associated with the stimulus-related activity from entropy produced by the modulation. To articulate this theory, we describe stimulus-evoked activity of a neural population based on the maximum entropy principle with constraints on two types of overlapping activities, one that is controlled by stimulus conditions and the other, termed internal activity, that is regulated internally in an organism. We demonstrate that modulation of the internal activity rea…
Most neurons in peripheral sensory pathways initially respond vigorously when a preferred stimulus is presented, but adapt as stimulation continues. It is unclear how this phenomenon affects stimulus representation in the later stages of cortical sensory processing. Here, we show that a temporally sparse and reliable stimulus representation develops naturally in a network with adapting neurons. We find that cellular adaptation plays a critical role in the transient reduction of the trial-by-trial variability of cortical spiking, providing an explanation for a wide-spread and hitherto unexplain…
The dynamical responses of complex neuronal networks to external stimulus injected on a \emph{single} neuron are investigated. Stimulating the largest-degree neuron in the network, it is found that as the intensity of the stimulus increases, the network will be transiting from the resting to firing states and then restoring to the resting state, showing a bounded firing region in the parameter space. Furthermore, it is found that as the coupling strength decreases, the firing region is gradually expanded and, at the weak couplings, separated into disconnected subregions. By a simplified networ…
Sensory neurons are often described in terms of a receptive field, that is, a linear kernel through which stimuli are filtered before they are further processed. If information transmission is assumed to proceed in a feedforward cascade, the receptive field may be interpreted as the external stimulus' profile maximizing neuronal output. The nervous system, however, contains many feedback loops, and sensory neurons filter more currents than the ones representing the transduced external stimulus. Some of the additional currents are generated by the output activity of the neuron itself, and there…
Various classes of neurons alternate between high-frequency discharges and silent intervals. This phenomenon is called burst firing. To analyze burst activity in an insect system, grasshopper auditory receptor neurons were recorded in vivo for several distinct stimulus types. The experimental data show that both burst probability and burst characteristics are strongly influenced by temporal modulations of the acoustic stimulus. The tendency to burst, hence, is not only determined by cell-intrinsic processes, but also by their interaction with the stimulus time course. We study this interaction…
Computation in the brain involves multiple types of neurons, yet the organizing principles for how these neurons work together remain unclear. Information theory has offered explanations for how different types of neurons can optimize the encoding of different stimulus features. However, recent experiments indicate that separate neuronal types exist that encode the same stimulus features, but do so with different thresholds. Here we show that the emergence of these types of neurons can be quantitatively described by the theory of transitions between different phases of matter. The two key para…
Spectral-Stimulus Information for Self-Supervised Stimulus Encoding
Department of Mathematics, The University of Tennessee, Knoxville, TN 37996, United States of America e5；Department of Computer, Data, \& Mathematical Sciences, Simmons University, Boston, MA 02115, United States of America e1；The U.S. Army Combat Capabilities Development Command Army Research Laboratory, Aberdeen Proving Ground, MD 21005, United States of America e2,e3,e4
The sensory-triggered activity of a neuron is typically characterized in terms of a tuning curve, which describes the neuron's average response as a function of a parameter that characterizes a physical stimulus. What determines the shapes of tuning curves in a neuronal population? Previous theoretical studies and related experiments suggest that many response characteristics of sensory neurons are optimal for encoding stimulus-related information. This notion, however, does not explain the two general types of tuning profiles that are commonly observed: unimodal and monotonic. Here, I quantif…
Stochastic integrate-and-fire (IF) neuron models have found widespread applications in computational neuroscience. Here we present results on the white-noise-driven perfect, leaky, and quadratic IF models, focusing on the spectral statistics (power spectra, cross spectra, and coherence functions) in different dynamical regimes (noise-induced and tonic firing regimes with low or moderate noise). We make the models comparable by tuning parameters such that the mean value and the coefficient of variation of the interspike interval match for all of them. We find that, under these conditions, the p…
Models of neural responses to stimuli with complex spatiotemporal correlation structure often assume that neurons are only selective for a small number of linear projections of a potentially high-dimensional input. Here we explore recent modeling approaches where the neural response depends on the quadratic form of the input rather than on its linear projection, that is, the neuron is sensitive to the local covariance structure of the signal preceding the spike. To infer this quadratic dependence in the presence of arbitrary (e.g. naturalistic) stimulus distribution, we review several inferenc…
Sensory neurons often have variable responses to repeated presentations of the same stimulus, which can significantly degrade the stimulus information contained in those responses. This information can in principle be preserved if variability is shared across many neurons, but depends on the structure of the shared variability and its relationship to sensory encoding at the population level. The structure of this shared variability in neural activity can be characterized by latent variable models, although they have thus far typically been used under restrictive mathematical assumptions. Here …
In the olfactory system, odor percepts retain their identity despite substantial variations in concentration, timing, and background. We propose a novel strategy for encoding intensity-invariant stimuli identity that is based on representing relative rather than absolute values of the stimulus features. Because, in this scheme, stimulus identity depends on relative amplitudes of stimulus features, identity becomes invariant with respect to variations in intensity and monotonous non-linearities of neuronal responses. In the olfactory system, stimulus identity can be represented by the identitie…
We demonstrate that two key theoretical objects used widely in Computational Neuroscience, the phase-resetting curve (PRC) from dynamics and the spike triggered average (STA) from statistical analysis, are closely related under a wide range of stimulus conditions. We prove that the STA is proportional to the derivative of the PRC. We compare these analytic results to numerical calculations for the Hodgkin-Huxley neuron and we apply the method to neurons in the olfactory bulb of mice. This observation allows us to relate the stimulus-response properties of a neuron to its dynamics, bridging the…
In the principal cells of the insect mushroom body, the Kenyon cells (KC), olfactory information is represented by a spatially and temporally sparse code. Each odor stimulus will activate only a small portion of neurons and each stimulus leads to only a short phasic response following stimulus onset irrespective of the actual duration of a constant stimulus. The mechanisms responsible for the sparse code in the KCs are yet unresolved. Here, we explore the role of the neuron-intrinsic mechanism of spike-frequency adaptation (SFA) in producing temporally sparse responses to sensory stimulation i…
The computation performed by a neuron can be formulated as a combination of dimensional reduction in stimulus space and the nonlinearity inherent in a spiking output. White noise stimulus and reverse correlation (the spike-triggered average and spike-triggered covariance) are often used in experimental neuroscience to `ask' neurons which dimensions in stimulus space they are sensitive to, and to characterize the nonlinearity of the response. In this paper, we apply reverse correlation to the simplest model neuron with temporal dynamics--the leaky integrate-and-fire model--and find that even fo…
Living organisms must actively maintain themselves in order to continue existing. Autopoiesis is a key concept in the study of living organisms, where the boundaries of the organism is not static by dynamically regulated by the system itself. To study the autonomous regulation of self-boundary, we focus on neural homeodynamic responses to environmental changes using both biological and artificial neural networks. Previous studies showed that embodied cultured neural networks and spiking neural networks with spike-timing dependent plasticity (STDP) learn an action as they avoid stimulation from…
Experiments that study neural encoding of stimuli at the level of individual neurons typically choose a small set of features present in the world --- contrast and luminance for vision, pitch and intensity for sound --- and assemble a stimulus set that systematically varies along these dimensions. Subsequent analysis of neural responses to these stimuli typically focuses on regression models, with experimenter-controlled features as predictors and spike counts or firing rates as responses. Unfortunately, this approach requires knowledge in advance about the relevant features coded by a given p…
The concept of feature selectivity in sensory signal processing can be formalized as dimensionality reduction: in a stimulus space of very high dimensions, neurons respond only to variations within some smaller, relevant subspace. But if neural responses exhibit invariances, then the relevant subspace typically cannot be reached by a Euclidean projection of the original stimulus. We argue that, in several cases, we can make progress by appealing to the simplest nonlinear construction, identifying the relevant variables as quadratic forms, or "stimulus energies." Natural examples include non-ph…
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…
The relationship between a neuron's complex inputs and its spiking output defines the neuron's coding strategy. This is frequently and effectively modeled phenomenologically by one or more linear filters that extract the components of the stimulus that are relevant for triggering spikes, and a nonlinear function that relates stimulus to firing probability. In many sensory systems, these two components of the coding strategy are found to adapt to changes in the statistics of the inputs, in such a way as to improve information transmission. Here, we show for two simple neuron models how feature …
We propose a method that would allow for a rigorous statistical analysis of neural responses to natural stimuli, which are non-Gaussian and exhibit strong correlations. We have in mind a model in which neurons are selective for a small number of stimulus dimensions out of the high dimensional stimulus space, but within this subspace the responses can be arbitrarily nonlinear. Existing analysis methods are based on correlation functions between stimuli and responses, but these methods are guaranteed to work only in the case of Gaussian stimulus ensembles. As an alternative to correlation functi…
Neural networks encode information through their collective spiking activity in response to external stimuli. This population response is noisy and strongly correlated, with complex interplay between correlations induced by the stimulus, and correlations caused by shared noise. Understanding how these correlations affect information transmission has so far been limited to pairs or small groups of neurons, because the curse of dimensionality impedes the evaluation of mutual information in larger populations. Here we develop a small-correlation expansion to compute the stimulus information carri…
We propose a method that allows for a rigorous statistical analysis of neural responses to natural stimuli which are non-Gaussian and exhibit strong correlations. We have in mind a model in which neurons are selective for a small number of stimulus dimensions out of a high dimensional stimulus space, but within this subspace the responses can be arbitrarily nonlinear. Existing analysis methods are based on correlation functions between stimuli and responses, but these methods are guaranteed to work only in the case of Gaussian stimulus ensembles. As an alternative to correlation functions, we …
We would like to know whether the statistics of neuronal responses vary across cortical areas. We examined stimulus-elicited spike count response distributions in V1 and IT cortices of awake monkeys. In both areas the distribution of spike counts for each stimulus was well-described by a Gaussian, with the log of the variance in the spike count linearly related to the log of the mean spike count. Two significant differences in response characteristics were found: both the range of spike counts and the slope of the log(variance) vs. log(mean) regression were larger in V1 than in IT. However, ne…
A neural code $\mathcal{C}$ is a collection of binary vectors of a given length n that record the co-firing patterns of a set of neurons. Our focus is on neural codes arising from place cells, neurons that respond to geographic stimulus. In this setting, the stimulus space can be visualized as subset of $\mathbb{R}^2$ covered by a collection $\mathcal{U}$ of convex sets such that the arrangement $\mathcal{U}$ forms an Euler diagram for $\mathcal{C}$. There are some methods to determine whether such a convex realization $\mathcal{U}$ exists; however, these methods do not describe how to draw a …
Local computation in microcircuits is an essential feature of distributed information processing in vertebrate and invertebrate brains. The insect antennal lobe represents a spatially confined local network that processes high-dimensional and redundant peripheral input to compute an efficient odor code. Social insects can rely on a particularly rich olfactory receptor repertoire and they exhibit complex odor-guided behaviors. This corresponds with a high anatomical complexity of their AL network. In the honeybee, a large number of glomeruli that receive sensory input are interconnected by a de…
Neurons in the main center of convergence in the auditory midbrain, the central nucleus of the inferior colliculus (ICC) have been shown to display either linear significant receptive fields, or both, linear and nonlinear significant receptive fields. In this study, we used reverse correlation to probe linear and nonlinear response properties of single neurons in the cat ICC. The receptive fields display areas of stimulus parameters leading to enhanced or inhibited spiking activity, and thus allow investigating the interplay to process complex sounds. Spiking responses were obtained from neura…
The nonselective cation channel TRPC4 has been shown to be present in high abundance in the corticolimbic regions of the brain and play a pivotal role in modulating cellular excitability due to their involvement in intracellular Ca2+ regulation. Recently we reported their involvement in socialization and regulating anxiety-like behaviors in rats. Given the important role for dopamine in modulating emotions involved in social anxiety we investigated whether TRPC4 protein and mRNA was found on dopaminergic neurons of the ventral tegmental area (VTA). Using emulsion autoradiography we found that …
Experimental data suggest that some classes of spiking neurons in the first layers of sensory systems are electrically coupled via gap junctions or ephaptic interactions. When the electrical coupling is removed, the response function (firing rate {\it vs.} stimulus intensity) of the uncoupled neurons typically shows a decrease in dynamic range and sensitivity. In order to assess the effect of electrical coupling in the sensory periphery, we calculate the response to a Poisson stimulus of a chain of excitable neurons modeled by $n$-state Greenberg-Hastings cellular automata in two approximation…
Redundancies and correlations in the responses of sensory neurons seem to waste neural resources but can carry cues about structured stimuli and may help the brain to correct for response errors. To assess how the retina negotiates this tradeoff, we measured simultaneous responses from populations of ganglion cells presented with natural and artificial stimuli that varied greatly in correlation structure. We found that pairwise correlations in the retinal output remained similar across stimuli with widely different spatio-temporal correlations including white noise and natural movies. Meanwhil…
Many biological systems can sense periodical variations in a stimulus input and produce well-timed, anticipatory responses after the input is removed. Such systems show memory effects for retaining timing information in the stimulus and cannot be understood from traditional synchronization consideration of passive oscillatory systems. To understand this anticipatory phenomena, we consider oscillators built from excitable systems with the addition of an adaptive dynamics. With such systems, well-timed post-stimulus responses similar to those from experiments can be obtained. Furthermore, a well…
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…
We review two examples where the linear response of a neuronal network submitted to an external stimulus can be derived explicitely, including network parameters dependence. This is done in a statistical physics-like approach where one associates to the spontaneous dynamics of the model a natural notion of Gibbs distribution inherited from ergodic theory or stochastic processes. These two examples are the Amari-Wilson-Cowan model and a conductance based Integrate and Fire model.
