Contextual modulation of orientation tuning contributes to efficient processing of natural stimuli

It has been proposed that sensory neurons are adapted to the statistical structure of the natural environment in order to encode natural stimuli efficiently. While spatiotemporal correlations in luminance signals may be decorrelated by neurons in early visual processing stages, higher-order correlations, such as those in the orientation domain, are likely to persist in the input representation until the cortical level. In this study, we first examine orientation correlations in natural stimuli across brief time intervals and across nearby regions of space, and find strong correlations in both domains. We then examine contextual modulation of orientation tuning. We find that both temporal and spatial contexts exert a common influence on orientation tuning, shifting tuning away from the orientation of either the adapting (temporal) or surrounding (spatial) grating. Finally, we incorporate this context-mediated repulsive shift in orientation tuning into a model of cortical responses. We find that a direct result of the shift is a reduction of the redundancy in the population responses evoked by the orientation configurations that are most common in natural stimuli. Thus, cortical neurons may be adapted to the statistics of orientation in natural stimuli in order to increase the efficiency of natural stimulus representation.     

Orientation tuning properties of simple cells in area V1 derived from an approximate analysis of nonlinear neural field models

We present a general approximation method for the mathematical analysis of spatially localized steady-state solutions in nonlinear neural field models. These models comprise several layers of excitatory and inhibitory cells. Coupling kernels between and inside layers are assumed to be gaussian shaped. In response to spatially localized (i.e., tuned) inputs, such networks typically reveal stationary localized activity profiles in the different layers. Qualitative properties of these solutions, like response amplitudes and tuning widths, are approximated for a whole class of nonlinear rate functions that obey a power law above some threshold and that are zero below. A special case of these functions is the semilinear function, which is commonly used in neural field models. The method is then applied to models for orientation tuning in cortical simple cells: first, to the one-layer model with "difference of gaussians" connectivity kernel developed by Carandini and Ringach (1997) as an abstraction of the biologically detailed simulations of Somers, Nelson, and Sur (1995); second, to a two-field model comprising excitatory and inhibitory cells in two separate layers. Under certain conditions, both models have the same steady states. Comparing simulations of the field models and results derived from the approximation method, we find that the approximation well predicts the tuning behavior of the full model. Moreover, explicit formulas for approximate amplitudes and tuning widths in response to changing input strength are given and checked numerically. Comparing the network behavior for different nonlinearities, we find that the only rate function (from the class of functions under study) that leads to constant tuning widths and a linear increase of firing rates in response to increasing input is the semilinear function. For other nonlinearities, the qualitative network response depends on whether the model neurons operate in a convex (e.g., x(2)) or concave (e.g., sqrt(x)) regime of their rate function. In the first case, tuning gradually changes from input driven at low input strength (broad tuning strongly depending on the input and roughly linear amplitudes in response to input strength) to recurrently driven at moderate input strength (sharp tuning, supralinear increase of amplitudes in response to input strength). For concave rate functions, the network reveals stable hysteresis between a state at low firing rates and a tuned state at high rates. This means that the network can "memorize" tuning properties of a previously shown stimulus. Sigmoid rate functions can combine both effects. In contrast to the Carandini-Ringach model, the two-field model further reveals oscillations with typical frequencies in the beta and gamma range, when the excitatory and inhibitory connections are relatively strong. This suggests a rhythmic modulation of tuning properties during cortical oscillations.     

Adaptive gain control for spike-based map communication in a neuromorphic vision system

To support large numbers of model neurons, neuromorphic vision systems are increasingly adopting a distributed architecture, where different arrays of neurons are located on different chips or processors. Spike-based protocols are used to communicate activity between processors. The spike activity in the arrays depends on the input statistics as well as internal parameters such as time constants and gains. In this paper, we investigate strategies for automatically adapting these parameters to maintain a constant firing rate in response to changes in the input statistics. We find that under the constraint of maintaining a fixed firing rate, a strategy based upon updating the gain alone performs as well as an optimal strategy where both the gain and the time constant are allowed to vary. We discuss how to choose the time constant and propose an adaptive gain control mechanism whose operation is robust to changes in the input statistics. Our experimental results on a mobile robotic platform validate the analysis and efficacy of the proposed strategy.     

Effect of lateral connections on the accuracy of the population code for a network of spiking neurons.

We study how neuronal connections in a population of spiking neurons affect the accuracy of stimulus estimation. Neurons in our model code for a one-dimensional orientation variable phi. Connectivity between two neurons depends on the absolute difference absolute value(phi - phi') between the preferred orientation of the two neurons. We derive an analytical expression of the activity profile for a population of neurons described by the spike response model with noisy threshold. We estimate the stimulus orientation and the trial-to-trial fluctuations using the population vector method. For stationary stimuli, uniform inhibitory connections produce a more reliable estimation of the stimulus than short-range excitatory connections with long-range inhibitions, although the latter interaction type produces a sharper tuning curve. These results are consistent with previous analytical studies of the Fisher information.     

A sparse generative model of V1 simple cells with intrinsic plasticity

Current models for learning feature detectors work on two timescales: on a fast timescale, the internal neurons' activations adapt to the current stimulus; on a slow timescale, the weights adapt to the statistics of the set of stimuli. Here we explore the adaptation of a neuron's intrinsic excitability, termed intrinsic plasticity, which occurs on a separate timescale. Here, a neuron maintains homeostasis of an exponentially distributed firing rate in a dynamic environment. We exploit this in the context of a generative model to impose sparse coding. With natural image input, localized edge detectors emerge as models of V1 simple cells. An intermediate timescale for the intrinsic plasticity parameters allows modeling aftereffects. In the tilt aftereffect, after a viewer adapts to a grid of a certain orientation, grids of a nearby orientation will be perceived as tilted away from the adapted orientation. Our results show that adapting the neurons' gain-parameter but not the threshold-parameter accounts for this effect. It occurs because neurons coding for the adapting stimulus attenuate their gain, while others increase it. Despite its simplicity and low maintenance, the intrinsic plasticity model accounts for more experimental details than previous models without this mechanism.     

Nonlinear population codes

Theoretical and experimental studies of distributed neuronal representations of sensory and behavioral variables usually assume that the tuning of the mean firing rates is the main source of information. However, recent theoretical studies have investigated the effect of cross-correlations in the trial-to-trial fluctuations of the neuronal responses on the accuracy of the representation. Assuming that only the first-order statistics of the neuronal responses are tuned to the stimulus, these studies have shown that in the presence of correlations, similar to those observed experimentally in cortical ensembles of neurons, the amount of information in the population is limited, yielding nonzero error levels even in the limit of infinitely large populations of neurons. In this letter, we study correlated neuronal populations whose higher-order statistics, and in particular response variances, are also modulated by the stimulus. Weask two questions: Does the correlated noise limit the accuracy of the neuronal representation of the stimulus? and, How can a biological mechanism extract most of the information embedded in the higher-order statistics of the neuronal responses? Specifically, we address these questions in the context of a population of neurons coding an angular variable. We show that the information embedded in the variances grows linearly with the population size despite the presence of strong correlated noise. This information cannot be extracted by linear readout schemes, including the linear population vector. Instead, we propose a bilinear readout scheme that involves spatial decorrelation, quadratic nonlinearity, and population vector summation. We show that this nonlinear population vector scheme yields accurate estimates of stimulus parameters, with an efficiency that grows linearly with the population size. This code can be implemented using biologically plausible neurons.     

Influences of synaptic location on the synchronization of rhythmic bursting neurons

We study how the location of synaptic input influences the stablex firing states in coupled model neurons bursting rhythmically at the gamma frequencies (20-70 Hz). The model neuron consists of two compartments and generates one, two, three or four spikes in each burst depending on the intensity of input current and the maximum conductance of M-type potassium current. If the somata are connected by reciprocal excitatory synapses, we find strong correlations between the changes in the bursting mode and those in the stable phase-locked states of the coupled neurons. The stability of the in-phase phase-locked state (synchronously firing state) tends to change when the individual neurons change their bursting patterns. If, however, the synaptic connections are terminated on the dendritic compartments, no such correlated changes occur. In this case, the coupled bursting neurons do not show the in-phase phase-locked state in any bursting mode. These results indicate that synchronization behaviour of bursting neurons significantly depends on the synaptic location, unlike a coupled system of regular spiking neurons.     

Theory of input spike auto- and cross-correlations and their effect on the response of spiking neurons

Spike correlations between neurons are ubiquitous in the cortex, but their role is not understood. Here we describe the firing response of a leaky integrate-and-fire neuron (LIF) when it receives a temporarily correlated input generated by presynaptic correlated neuronal populations. Input correlations are characterized in terms of the firing rates, Fano factors, correlation coefficients, and correlation timescale of the neurons driving the target neuron. We show that the sum of the presynaptic spike trains cannot be well described by a Poisson process. In fact, the total input current has a nontrivial two-point correlation function described by two main parameters: the correlation timescale (how precise the input correlations are in time) and the correlation magnitude (how strong they are). Therefore, the total current generated by the input spike trains is not well described by a white noise gaussian process. Instead, we model the total current as a colored gaussian process with the same mean and two-point correlation function, leading to the formulation of the problem in terms of a Fokker-Planck equation. Solutions of the output firing rate are found in the limit of short and long correlation timescales. The solutions described here expand and improve on our previous results (Moreno, de la Rocha, Renart, & Parga, 2002) by presenting new analytical expressions for the output firing rate for general IF neurons, extending the validity of the results for arbitrarily large correlation magnitude, and by describing the differential effect of correlations on the mean-driven or noise-dominated firing regimes. Also the details of this novel formalism are given here for the first time. We employ numerical simulations to confirm the analytical solutions and study the firing response to sudden changes in the input correlations. We expect this formalism to be useful for the study of correlations in neuronal networks and their role in neural processing and information transmission.     

Higher-order statistics of input ensembles and the response of simple model neurons

Pairwise correlations among spike trains recorded in vivo have been frequently reported. It has been argued that correlated activity could play an important role in the brain, because it efficiently modulates the response of a postsynaptic neuron. We show here that a neuron's output firing rate critically depends on the higher-order statistics of the input ensemble. We constructed two statistical models of populations of spiking neurons that fired with the same rates and had identical pairwise correlations, but differed with regard to the higher-order interactions within the population. The first ensemble was characterized by clusters of spikes synchronized over the whole population. In the second ensemble, the size of spike clusters was, on average, proportional to the pairwise correlation. For both input models, we assessed the role of the size of the population, the firing rate, and the pairwise correlation on the output rate of two simple model neurons: a continuous firing-rate model and a conductance-based leaky integrate-and-fire neuron. An approximation to the mean output rate of the firing-rate neuron could be derived analytically with the help of shot noise theory. Interestingly, the essential features of the mean response of the two neuron models were similar. For both neuron models, the three input parameters played radically different roles with respect to the postsynaptic firing rate, depending on the interaction structure of the input. For instance, in the case of an ensemble with small and distributed spike clusters, the output firing rate was efficiently controlled by the size of the input population. In addition to the interaction structure, the ratio of inhibition to excitation was found to strongly modulate the effect of correlation on the postsynaptic firing rate.     

Analytic expressions for rate and CV of a type I neuron driven by white gaussian noise

We study the one-dimensional normal form of a saddle-node system under the influence of additive gaussian white noise and a static "bias current" input parameter, a model that can be looked upon as the simplest version of a type I neuron with stochastic input. This is in contrast with the numerous studies devoted to the noise-driven leaky integrate-and-fire neuron. We focus on the firing rate and coefficient of variation (CV) of the interspike interval density, for which scaling relations with respect to the input parameter and noise intensity are derived. Quadrature formulas for rate and CV are numerically evaluated and compared to numerical simulations of the system and to various approximation formulas obtained in different limiting cases of the model. We also show that caution must be used to extend these results to the Theta neuron model with multiplicative gaussian white noise. The correspondence between the first passage time statistics for the saddle-node model and the Theta neuron model is obtained only in the Stratonovich interpretation of the stochastic Theta neuron model, while previous results have focused only on the Ito interpretation. The correct Stratonovich interpretation yields CVs that are still relatively high, although smaller than in the Ito interpretation; it also produces certain qualitative differences, especially at larger noise intensities. Our analysis provides useful relations for assessing the distance to threshold and the level of synaptic noise in real type I neurons from their firing statistics. We also briefly discuss the effect of finite boundaries (finite values of threshold and reset) on the firing statistics.     

Dynamical mechanism for sharp orientation tuning in an integrate-and-fire model of a cortical hypercolumn

Orientation tuning in a ring of pulse-coupled integrate-and-fire (IF) neurons is analyzed in terms of spontaneous pattern formation. It is shown how the ring bifurcates from a synchronous state to a non-phase-locked state whose spike trains are characterized by clustered but irregular fluctuations of the interspike intervals (ISIs). The separation of these clusters in phase space results in a localized peak of activity as measured by the time-averaged firing rate of the neurons. This generates a sharp orientation tuning curve that can lock to a slowly rotating, weakly tuned external stimulus. Under certain conditions, the peak can slowly rotate even to a fixed external stimulus. The ring also exhibits hysteresis due to the subcritical nature of the bifurcation to sharp orientation tuning. Such behavior is shown to be consistent with a corresponding analog version of the IF model in the limit of slow synaptic interactions. For fast synapses, the deterministic fluctuations of the ISIs associated with the tuning curve can support a coefficient of variation of order unity.     

Correlation between uncoupled conductance-based integrate-and-fire neurons due to common and synchronous presynaptic firing

We investigate the firing characteristics of conductance-based integrate-and-fire neurons and the correlation of firing for uncoupled pairs of neurons as a result of common input and synchronous firing of multiple synaptic inputs. Analytical approximations are derived for the moments of the steady state potential and the effective time constant. We show that postsynaptic firing barely depends on the correlation between inhibitory inputs; only the inhibitory firing rate matters. In contrast, both the degree of synchrony and the firing rate of excitatory inputs are relevant. A coefficient of variation CV > 1 can be attained with low inhibitory firing rates and (Poisson-modulated) synchronized excitatory synaptic input, where both the number of presynaptic neurons in synchronous firing assemblies and the synchronous firing rate should be sufficiently large. The correlation in firing of a pair of uncoupled neurons due to common excitatory input is initially increased for increasing firing rates of independent inhibitory inputs but decreases for large inhibitory firing rates. Common inhibitory input to a pair of uncoupled neurons barely induces correlated firing, but amplifies the effect of common excitation. Synchronous firing assemblies in the common input further enhance the correlation and are essential to attain experimentally observed correlation values. Since uncorrelated common input (i.e., common input by neurons, which do not fire in synchrony) cannot induce sufficient postsynaptic correlation, we conclude that lateral couplings are essential to establish clusters of synchronously firing neurons.     

Information encoding and computation with spikes and bursts

Neurons compute and communicate by transforming synaptic input patterns into output spike trains. The nature of this transformation depends crucially on the properties of voltage-gated conductances in neuronal membranes. These intrinsic membrane conductances can enable neurons to generate different spike patterns including brief, high-frequency bursts that are commonly observed in a variety of brain regions. Here we examine how the membrane conductances that generate bursts affect neural computation and encoding. We simulated a bursting neuron model driven by random current input signal and superposed noise. We consider two issues: the timing reliability of different spike patterns and the computation performed by the neuron. Statistical analysis of the simulated spike trains shows that the timing of bursts is much more precise than the timing of single spikes. Furthermore, the number of spikes per burst is highly robust to noise. Next we considered the computation performed by the neuron: how different features of the input current are mapped into specific output spike patterns. Dimensional reduction and statistical classification techniques were used to determine the stimulus features triggering different firing patterns. Our main result is that spikes, and bursts of different durations, code for different stimulus features, which can be quantified without a priori assumptions about those features. These findings lead us to propose that the biophysical mechanisms of spike generation enables individual neurons to encode different stimulus features into distinct spike patterns.     

Determination of firing times for the stochastic Fitzhugh-Nagumo neuronal model

We present for the first time an analytical approach for determining the time of firing of multicomponent nonlinear stochastic neuronal models. We apply the theory of first exit times for Markov processes to the Fitzhugh-Nagumo system with a constant mean gaussian white noise input, representing stochastic excitation and inhibition. Partial differential equations are obtained for the moments of the time to first spike. The observation that the recovery variable barely changes in the prespike trajectory leads to an accurate one-dimensional approximation. For the moments of the time to reach threshold, this leads to ordinary differential equations that may be easily solved. Several analytical approaches are explored that involve perturbation expansions for large and small values of the noise parameter. For ranges of the parameters appropriate for these asymptotic methods, the perturbation solutions are used to establish the validity of the one-dimensional approximation for both small and large values of the noise parameter. Additional verification is obtained with the excellent agreement between the mean and variance of the firing time found by numerical solution of the differential equations for the one-dimensional approximation and those obtained by simulation of the solutions of the model stochastic differential equations. Such agreement extends to intermediate values of the noise parameter. For the mean time to threshold, we find maxima at small noise values that constitute a form of stochastic resonance. We also investigate the dependence of the mean firing time on the initial values of the voltage and recovery variables when the input current has zero mean.     

Population density methods for stochastic neurons with realistic synaptic kinetics: firing rate dynamics and fast computational methods

An outstanding problem in computational neuroscience is how to use population density function (PDF) methods to model neural networks with realistic synaptic kinetics in a computationally efficient manner. We explore an application of two-dimensional (2-D) PDF methods to simulating electrical activity in networks of excitatory integrate-and-fire neurons.We formulate a pair of coupled partial differential-integral equations describing the evolution of PDFs for neurons in non-refractory and refractory pools. The population firing rate is given by the total flux of probability across the threshold voltage. We use an operator-splitting method to reduce computation time. We report on speed and accuracy of PDF results and compare them to those from direct, Monte-Carlo simulations.We compute temporal frequency response functions for the transduction from the rate of postsynaptic input to population firing rate, and examine its dependence on background synaptic input rate. The behaviors in the1-D and 2-D cases--corresponding to instantaneous and non-instantaneous synaptic kinetics, respectively--differ markedly from those for a somewhat different transduction: from injected current input to population firing rate output (Brunel et al. 2001; Fourcaud & Brunel 2002).We extend our method by adding inhibitory input, consider a 3-D to 2-D dimension reduction method, demonstrate its limitations, and suggest directions for future study.     

Dynamic gain changes during attentional modulation

Attention causes a multiplicative effect on firing rates of cortical neurons without affecting their selectivity (Motter, 1993; McAdams & Maunsell, 1999a) or the relationship between the spike count mean and variance (McAdams & Maunsell, 1999b). We analyzed attentional modulation of the firing rates of 144 neurons in the secondary somatosensory cortex (SII) of two monkeys trained to switch their attention between a tactile pattern recognition task and a visual task. We found that neurons in SII cortex also undergo a predominantly multiplicative modulation in firing rates without affecting the ratio of variance to mean firing rate (i.e., the Fano factor). Furthermore, both additive and multiplicative components of attentional modulation varied dynamically during the stimulus presentation. We then used a standard conductance-based integrate-and-fire model neuron to ascertain which mechanisms might account for a multiplicative increase in firing rate without affecting the Fano factor. Six mechanisms were identified as biophysically plausible ways that attention could modify the firing rate: spike threshold, firing rate adaptation, excitatory input synchrony, synchrony between all inputs, membrane leak resistance, and reset potential. Of these, only a change in spike threshold or in firing rate adaptation affected model firing rates in a manner compatible with the observed neural data. The results indicate that only a limited number of biophysical mechanisms can account for observed attentional modulation.     

Mean-driven and fluctuation-driven persistent activity in recurrent networks

Spike trains from cortical neurons show a high degree of irregularity, with coefficients of variation (CV) of their interspike interval (ISI) distribution close to or higher than one. It has been suggested that this irregularity might be a reflection of a particular dynamical state of the local cortical circuit in which excitation and inhibition balance each other. In this "balanced" state, the mean current to the neurons is below threshold, and firing is driven by current fluctuations, resulting in irregular Poisson-like spike trains. Recent data show that the degree of irregularity in neuronal spike trains recorded during the delay period of working memory experiments is the same for both low-activity states of a few Hz and for elevated, persistent activity states of a few tens of Hz. Since the difference between these persistent activity states cannot be due to external factors coming from sensory inputs, this suggests that the underlying network dynamics might support coexisting balanced states at different firing rates. We use mean field techniques to study the possible existence of multiple balanced steady states in recurrent networks of current-based leaky integrate-and-fire (LIF) neurons. To assess the degree of balance of a steady state, we extend existing mean-field theories so that not only the firing rate, but also the coefficient of variation of the interspike interval distribution of the neurons, are determined self-consistently. Depending on the connectivity parameters of the network, we find bistable solutions of different types. If the local recurrent connectivity is mainly excitatory, the two stable steady states differ mainly in the mean current to the neurons. In this case, the mean drive in the elevated persistent activity state is suprathreshold and typically characterized by low spiking irregularity. If the local recurrent excitatory and inhibitory drives are both large and nearly balanced, or even dominated by inhibition, two stable states coexist, both with subthreshold current drive. In this case, the spiking variability in both the resting state and the mnemonic persistent state is large, but the balance condition implies parameter fine-tuning. Since the degree of required fine-tuning increases with network size and, on the other hand, the size of the fluctuations in the afferent current to the cells increases for small networks, overall we find that fluctuation-driven persistent activity in the very simplified type of models we analyze is not a robust phenomenon. Possible implications of considering more realistic models are discussed.     

Modeling short-term adaptation processes of visual motion detectors

In the brain, both neural processing dynamics as well as the perceptual interpretation of a stimulus can depend on sensory history. The underlying principle is a sensory adaptation to the statistics of the input collected over some timespan, allowing the system to tune its detectors, e.g. by better sampling the input space and adjusting the response. Here, we show how a model for adaptation in visual motion processing can be set up from first principles using a generative formulation and casting the problem of adaptation in terms of optimal estimation over time. The model leads to an online adaptation of velocity tuning curves, inducing shifts in the velocity tuning and changes in the tuning curve widths that are compatible with observations from physiological experiments on macaque MT neurons. We also show how such an adaptation leads to a greater computational efficiency by a better sampling of the velocity space, requiring less motion detectors to achieve a desired level of estimation accuracy.     

Optimal tuning widths in population coding of periodic variables

We study the relationship between the accuracy of a large neuronal population in encoding periodic sensory stimuli and the width of the tuning curves of individual neurons in the population. By using general simple models of population activity, we show that when considering one or two periodic stimulus features, a narrow tuning width provides better population encoding accuracy. When encoding more than two periodic stimulus features, the information conveyed by the population is instead maximal for finite values of the tuning width. These optimal values are only weakly dependent on model parameters and are similar to the width of tuning to orientation or motion direction of real visual cortical neurons. A very large tuning width leads to poor encoding accuracy, whatever the number of stimulus features encoded. Thus, optimal coding of periodic stimuli is different from that of nonperiodic stimuli, which, as shown in previous studies, would require infinitely large tuning widths when coding more than two stimulus features.