Natural Stimulus Statistics Research Articles

Neural populations within macaque early vestibular pathways are adapted to encode natural self-motion.

How the activities of large neural populations are integrated in the brain to ensure accurate perception and behavior remains a central problem in systems neuroscience. Here, we investigated population coding of naturalistic self-motion by neurons within early vestibular pathways in rhesus macaques (Macacca mulatta). While vestibular neurons displayed similar dynamic tuning to self-motion, inspection of their spike trains revealed significant heterogeneity. Further analysis revealed that, during natural but not artificial stimulation, heterogeneity resulted primarily from variability across neurons as opposed to trial-to-trial variability. Interestingly, vestibular neurons displayed different correlation structures during naturalistic and artificial self-motion. Specifically, while correlations due to the stimulus (i.e., signal correlations) did not differ, correlations between the trial-to-trial variabilities of neural responses (i.e., noise correlations) were instead significantly positive during naturalistic but not artificial stimulation. Using computational modeling, we show that positive noise correlations during naturalistic stimulation benefits information transmission by heterogeneous vestibular neural populations. Taken together, our results provide evidence that neurons within early vestibular pathways are adapted to the statistics of natural self-motion stimuli at the population level. We suggest that similar adaptations will be found in other systems and species.

Rat sensitivity to multipoint statistics is predicted by efficient coding of natural scenes.

Efficient processing of sensory data requires adapting the neuronal encoding strategy to the statistics of natural stimuli. Previously, in Hermundstad et al., 2014, we showed that local multipoint correlation patterns that are most variable in natural images are also the most perceptually salient for human observers, in a way that is compatible with the efficient coding principle. Understanding the neuronal mechanisms underlying such adaptation to image statistics will require performing invasive experiments that are impossible in humans. Therefore, it is important to understand whether a similar phenomenon can be detected in animal species that allow for powerful experimental manipulations, such as rodents. Here we selected four image statistics (from single- to four-point correlations) and trained four groups of rats to discriminate between white noise patterns and binary textures containing variable intensity levels of one of such statistics. We interpreted the resulting psychometric data with an ideal observer model, finding a sharp decrease in sensitivity from two- to four-point correlations and a further decrease from four- to three-point. This ranking fully reproduces the trend we previously observed in humans, thus extending a direct demonstration of efficient coding to a species where neuronal and developmental processes can be interrogated and causally manipulated.

A Neural Representation of Naturalistic Motion-Guided Behavior in the Zebrafish Brain

All animals must transform ambiguous sensory data into successful behavior. This requires sensory representations that accurately reflect the statistics of natural stimuli and behavior. Multiple studies show that visual motion processing is tuned for accuracy under naturalistic conditions, but the sensorimotor circuits extracting these cues and implementing motion-guided behavior remain unclear. Here we show that the larval zebrafish retina extracts a diversity of naturalistic motion cues, and the retinorecipient pretectum organizes these cues around the elements of behavior. We find that higher-order motion stimuli, gliders, induce optomotor behavior matching expectations from natural scene analyses. We then image activity of retinal ganglion cell terminals and pretectal neurons. The retina exhibits direction-selective responses across glider stimuli, and anatomically clustered pretectal neurons respond with magnitudes matching behavior. Peripheral computations thus reflect natural input statistics, whereas central brain activity precisely codes information needed for behavior. This general principle could organize sensorimotor transformations across animal species.

Ecological origins of perceptual grouping principles in the auditory system.

Events and objects in the world must be inferred from sensory signals to support behavior. Because sensory measurements are temporally and spatially local, the estimation of an object or event can be viewed as the grouping of these measurements into representations of their common causes. Perceptual grouping is believed to reflect internalized regularities of the natural environment, yet grouping cues have traditionally been identified using informal observation and investigated using artificial stimuli. The relationship of grouping to natural signal statistics has thus remained unclear, and additional or alternative cues remain possible. Here, we develop a general methodology for relating grouping to natural sensory signals and apply it to derive auditory grouping cues from natural sounds. We first learned local spectrotemporal features from natural sounds and measured their co-occurrence statistics. We then learned a small set of stimulus properties that could predict the measured feature co-occurrences. The resulting cues included established grouping cues, such as harmonic frequency relationships and temporal coincidence, but also revealed previously unappreciated grouping principles. Human perceptual grouping was predicted by natural feature co-occurrence, with humans relying on the derived grouping cues in proportion to their informativity about co-occurrence in natural sounds. The results suggest that auditory grouping is adapted to natural stimulus statistics, show how these statistics can reveal previously unappreciated grouping phenomena, and provide a framework for studying grouping in natural signals.

Functional diversity among sensory neurons from efficient coding principles.

In many sensory systems the neural signal is coded by the coordinated response of heterogeneous populations of neurons. What computational benefit does this diversity confer on information processing? We derive an efficient coding framework assuming that neurons have evolved to communicate signals optimally given natural stimulus statistics and metabolic constraints. Incorporating nonlinearities and realistic noise, we study optimal population coding of the same sensory variable using two measures: maximizing the mutual information between stimuli and responses, and minimizing the error incurred by the optimal linear decoder of responses. Our theory is applied to a commonly observed splitting of sensory neurons into ON and OFF that signal stimulus increases or decreases, and to populations of monotonically increasing responses of the same type, ON. Depending on the optimality measure, we make different predictions about how to optimally split a population into ON and OFF, and how to allocate the firing thresholds of individual neurons given realistic stimulus distributions and noise, which accord with certain biases observed experimentally.

Neuronal variability and tuning are balanced to optimize naturalistic self-motion coding in primate vestibular pathways.

It is commonly assumed that the brain's neural coding strategies are adapted to the statistics of natural stimuli. Specifically, to maximize information transmission, a sensory neuron's tuning function should effectively oppose the decaying stimulus spectral power, such that the neural response is temporally decorrelated (i.e. 'whitened'). However, theory predicts that the structure of neuronal variability also plays an essential role in determining how coding is optimized. Here, we provide experimental evidence supporting this view by recording from neurons in early vestibular pathways during naturalistic self-motion. We found that central vestibular neurons displayed temporally whitened responses that could not be explained by their tuning alone. Rather, computational modeling and analysis revealed that neuronal variability and tuning were matched to effectively complement natural stimulus statistics, thereby achieving temporal decorrelation and optimizing information transmission. Taken together, our findings reveal a novel strategy by which neural variability contributes to optimized processing of naturalistic stimuli.

Feedback optimizes neural coding and perception of natural stimuli.

Growing evidence suggests that sensory neurons achieve optimal encoding by matching their tuning properties to the natural stimulus statistics. However, the underlying mechanisms remain unclear. Here we demonstrate that feedback pathways from higher brain areas mediate optimized encoding of naturalistic stimuli via temporal whitening in the weakly electric fish Apteronotus leptorhynchus. While one source of direct feedback uniformly enhances neural responses, a separate source of indirect feedback selectively attenuates responses to low frequencies, thus creating a high-pass neural tuning curve that opposes the decaying spectral power of natural stimuli. Additionally, we recorded from two populations of higher brain neurons responsible for the direct and indirect descending inputs. While one population displayed broadband tuning, the other displayed high-pass tuning and thus performed temporal whitening. Hence, our results demonstrate a novel function for descending input in optimizing neural responses to sensory input through temporal whitening that is likely to be conserved across systems and species.

Fast intensity adaptation enhances the encoding of sound in Drosophila

To faithfully encode complex stimuli, sensory neurons should correct, via adaptation, for stimulus properties that corrupt pattern recognition. Here we investigate sound intensity adaptation in the Drosophila auditory system, which is largely devoted to processing courtship song. Mechanosensory neurons (JONs) in the antenna are sensitive not only to sound-induced antennal vibrations, but also to wind or gravity, which affect the antenna’s mean position. Song pattern recognition, therefore, requires adaptation to antennal position (stimulus mean) in addition to sound intensity (stimulus variance). We discover fast variance adaptation in Drosophila JONs, which corrects for background noise over the behaviorally relevant intensity range. We determine where mean and variance adaptation arises and how they interact. A computational model explains our results using a sequence of subtractive and divisive adaptation modules, interleaved by rectification. These results lay the foundation for identifying the molecular and biophysical implementation of adaptation to the statistics of natural sensory stimuli.

Learning Midlevel Auditory Codes from Natural Sound Statistics.

Interaction with the world requires an organism to transform sensory signals into representations in which behaviorally meaningful properties of the environment are made explicit. These representations are derived through cascades of neuronal processing stages in which neurons at each stage recode the output of preceding stages. Explanations of sensory coding may thus involve understanding how low-level patterns are combined into more complex structures. To gain insight into such midlevel representations for sound, we designed a hierarchical generative model of natural sounds that learns combinations of spectrotemporal features from natural stimulus statistics. In the first layer, the model forms a sparse convolutional code of spectrograms using a dictionary of learned spectrotemporal kernels. To generalize from specific kernel activation patterns, the second layer encodes patterns of time-varying magnitude of multiple first-layer coefficients. When trained on corpora of speech and environmental sounds, some second-layer units learned to group similar spectrotemporal features. Others instantiate opponency between distinct sets of features. Such groupings might be instantiated by neurons in the auditory cortex, providing a hypothesis for midlevel neuronal computation.

Envelope statistics of self-motion signals experienced by human subjects during everyday activities: Implications for vestibular processing.

There is accumulating evidence that the brain’s neural coding strategies are constrained by natural stimulus statistics. Here we investigated the statistics of the time varying envelope (i.e. a second-order stimulus attribute that is related to variance) of rotational and translational self-motion signals experienced by human subjects during everyday activities. We found that envelopes can reach large values across all six motion dimensions (~450 deg/s for rotations and ~4 G for translations). Unlike results obtained in other sensory modalities, the spectral power of envelope signals decreased slowly for low (< 2 Hz) and more sharply for high (>2 Hz) temporal frequencies and thus was not well-fit by a power law. We next compared the spectral properties of envelope signals resulting from active and passive self-motion, as well as those resulting from signals obtained when the subject is absent (i.e. external stimuli). Our data suggest that different mechanisms underlie deviation from scale invariance in rotational and translational self-motion envelopes. Specifically, active self-motion and filtering by the human body cause deviation from scale invariance primarily for translational and rotational envelope signals, respectively. Finally, we used well-established models in order to predict the responses of peripheral vestibular afferents to natural envelope stimuli. We found that irregular afferents responded more strongly to envelopes than their regular counterparts. Our findings have important consequences for understanding the coding strategies used by the vestibular system to process natural second-order self-motion signals.

Optimized Parallel Coding of Second-Order Stimulus Features by Heterogeneous Neural Populations.

Efficient processing of sensory input is essential to ensure an organism's survival in its natural environment. Growing evidence suggests that sensory neurons can optimally encode natural stimuli by ensuring that their tuning opposes stimulus statistics, such that the resulting neuronal response contains equal power at all frequencies (i.e., is "white"). Such temporal decorrelation or whitening has been observed across modalities, but the effects of neural heterogeneities on determining tuning and thus responses to natural stimuli have not been investigated. Here, we investigate how heterogeneities in sensory pyramidal neurons organized in three parallel maps representing the body surface determine responses to second-order electrosensory stimulus features in the weakly electric fish Apteronotus leptorhynchus While some sources of heterogeneities such as ON- and OFF-type responses to first-order did not affect responses to second-order electrosensory stimulus features, other sources of heterogeneity within and across the maps strongly determined responses. We found that these cells effectively performed a fractional differentiation operation on their input with exponents ranging from zero (no differentiation) to 0.4 (strong differentiation). Varying adaptation in a simple model explained these heterogeneities and predicted a strong correlation between fractional differentiation and adaptation. Using natural stimuli, we found that only a small fraction of neurons implemented temporal whitening. Rather, a large fraction of neurons did not perform any significant whitening and thus preserved natural input statistics in their responses. We propose that this information is needed to properly decode optimized information sent in parallel through temporally whitened responses based on context. We demonstrate that heterogeneities in the same sensory neuron type can either have no or significant influence on their responses to second-order stimulus features. While an ON- or OFF-type response to first-order stimulus attributes has no significant influence on responses to second-order stimulus features, we found that only a small fraction of sensory neurons optimally encoded natural stimuli through high-pass filtering, thereby implementing temporal whitening. Surprisingly, a large fraction of sensory neurons performed little if no filtering of stimuli, thereby preserving natural stimulus statistics. We hypothesize that this pathway is necessary to properly decode optimized information contained in temporally whitened responses based on context.

Temporal decorrelation by SK channels enables efficient neural coding and perception of natural stimuli.

It is commonly assumed that neural systems efficiently process natural sensory input. However, the mechanisms by which such efficient processing is achieved, and the consequences for perception and behaviour remain poorly understood. Here we show that small conductance calcium-activated potassium (SK) channels enable efficient neural processing and perception of natural stimuli. Specifically, these channels allow for the high-pass filtering of sensory input, thereby removing temporal correlations or, equivalently, whitening frequency response power. Varying the degree of adaptation through pharmacological manipulation of SK channels reduced efficiency of coding of natural stimuli, which in turn gave rise to predictable changes in behavioural responses that were no longer matched to natural stimulus statistics. Our results thus demonstrate a novel mechanism by which the nervous system can implement efficient processing and perception of natural sensory input that is likely to be shared across systems and species.

Dynamical sensory representations establish a rapid odor code in a spiking model of the insect olfactory system

In their natural environment, animals sense and evaluate olfactory cues of time-varying composition and concentration. Their olfactory pathways are adapted to the natural stimulus statistics, thus it is not surprising that odor processing is fast [1]. Honey bees, for example, learn to discriminate odors presented as short as 200 ms [2]. The neural odor code in these animals emerges within 50ms after stimulus onset and neural representation changes dynamically during and after an odorant is present [1,3]. How is the insect olfactory system optimized to reliably estimate spatial and temporal aspects of the olfactory environment and what are the mechanisms behind rapid odor processing? To investigate odor encoding at the Antennal Lobe (AL) and the Mushroom Body (MB) level, we employ a simple phenomenological spiking network model of the honeybee olfactory system. The model implements a transformation from a low dimensional dense odorant representation in the AL to a high dimensional sparse representation in the MB. We demonstrate how information about the stimulus is present in both encoding schemes, by time resolved classification of neural activity. Our model displays sparse and robust odor representation in the Mushroom Body [4]. Typically, less than 10% of the Kenyon Cell population is activated by an odor, with only 2-3 spikes at the odor onset (Figure ​(Figure1A).1A). KC spikes establish a rapid odor identity code at stimulus onset, while intrinsic adaptation currents provide a persistent and prolonged odor trace (Figure ​(Figure1B).1B). Our approach allows us to investigate dynamical changes in odor representations and predict odor after images. Figure 1 (A) Kenyon Cell spike raster plot. Stimulation is indicated by gray shading (B) Top: Decoding Accuracy given two odors (chance level: 0.5) as a function of time based on spike count estimates in 50ms time bins. Bottom: Decoding accuracy based on KC adaptation ...

The opponent channel population code of sound location is an efficient representation of natural binaural sounds.

In mammalian auditory cortex, sound source position is represented by a population of broadly tuned neurons whose firing is modulated by sounds located at all positions surrounding the animal. Peaks of their tuning curves are concentrated at lateral position, while their slopes are steepest at the interaural midline, allowing for the maximum localization accuracy in that area. These experimental observations contradict initial assumptions that the auditory space is represented as a topographic cortical map. It has been suggested that a “panoramic” code has evolved to match specific demands of the sound localization task. This work provides evidence suggesting that properties of spatial auditory neurons identified experimentally follow from a general design principle- learning a sparse, efficient representation of natural stimuli. Natural binaural sounds were recorded and served as input to a hierarchical sparse-coding model. In the first layer, left and right ear sounds were separately encoded by a population of complex-valued basis functions which separated phase and amplitude. Both parameters are known to carry information relevant for spatial hearing. Monaural input converged in the second layer, which learned a joint representation of amplitude and interaural phase difference. Spatial selectivity of each second-layer unit was measured by exposing the model to natural sound sources recorded at different positions. Obtained tuning curves match well tuning characteristics of neurons in the mammalian auditory cortex. This study connects neuronal coding of the auditory space with natural stimulus statistics and generates new experimental predictions. Moreover, results presented here suggest that cortical regions with seemingly different functions may implement the same computational strategy-efficient coding.

The increased sensitivity of irregular peripheral canal and otolith vestibular afferents optimizes their encoding of natural stimuli.

Efficient processing of incoming sensory input is essential for an organism's survival. A growing body of evidence suggests that sensory systems have developed coding strategies that are constrained by the statistics of the natural environment. Consequently, it is necessary to first characterize neural responses to natural stimuli to uncover the coding strategies used by a given sensory system. Here we report for the first time the statistics of vestibular rotational and translational stimuli experienced by rhesus monkeys during natural (e.g., walking, grooming) behaviors. We find that these stimuli can reach intensities as high as 1500 deg/s and 8 G. Recordings from afferents during naturalistic rotational and linear motion further revealed strongly nonlinear responses in the form of rectification and saturation, which could not be accurately predicted by traditional linear models of vestibular processing. Accordingly, we used linear-nonlinear cascade models and found that these could accurately predict responses to naturalistic stimuli. Finally, we tested whether the statistics of natural vestibular signals constrain the neural coding strategies used by peripheral afferents. We found that both irregular otolith and semicircular canal afferents, because of their higher sensitivities, were more optimized for processing natural vestibular stimuli as compared with their regular counterparts. Our results therefore provide the first evidence supporting the hypothesis that the neural coding strategies used by the vestibular system are matched to the statistics of natural stimuli.

Variance predicts salience in central sensory processing.

Information processing in the sensory periphery is shaped by natural stimulus statistics. In the periphery, a transmission bottleneck constrains performance; thus efficient coding implies that natural signal components with a predictably wider range should be compressed. In a different regime--when sampling limitations constrain performance--efficient coding implies that more resources should be allocated to informative features that are more variable. We propose that this regime is relevant for sensory cortex when it extracts complex features from limited numbers of sensory samples. To test this prediction, we use central visual processing as a model: we show that visual sensitivity for local multi-point spatial correlations, described by dozens of independently-measured parameters, can be quantitatively predicted from the structure of natural images. This suggests that efficient coding applies centrally, where it extends to higher-order sensory features and operates in a regime in which sensitivity increases with feature variability.

A Bayesian observer model constrained by efficient coding accounts for both attractive and repulsive biases

Bayesian observer models have been quite successful in accounting for perceptual behavior. However, it is a common challenge to specify the two fundamental components of a Bayesian model, the prior distribution and the likelihood function, because they are formally unconstrained. We argue that a perceptual system that is adapted to the statistical structure of its environment naturally imposes constraints on its corresponding Bayesian model description. In particular, we assume the prior to reflect the stimulus distribution and the likelihood to be constrained by a sensory representation that is efficient. We show that these assumptions lead to an observer model that makes two counter-intuitive predictions: First, perceptual biases can be repulsive (i.e. biased away from the peak of the prior), which is in stark contrast to the traditional Bayesian view. Second, the model predicts that neural and stimulus noise are differentially affecting perceptual bias, with larger neural noise leading to an increase in repulsive bias while larger stimulus noise leading to a decrease. We tested our model against reported experimental data regarding two perceptual variables for which the natural stimulus statistics are known (orientation and spatial frequency of visual stimuli). We found that the model predicts the reported repulsive biases from the cardinal orientations and low spatial frequencies, respectively. Furthermore, it also accounts for the observed increase in bias with increasing levels of neural noise, as well as the relative attractive bias when comparing stimuli with high versus low stimulus noise. The model is capable of making quantitative predictions up to a scaling factor for any perceptual variable for which the stimulus statistics are known. Our results suggest that efficient coding provides a powerful constraint in specifying Bayesian observer models, and leads to successful predictions of perceptual effects that have been considered incompatible with the Bayesian framework. Meeting abstract presented at VSS 2014

Statistics of the vestibular input experienced during natural self-motion: implications for neural processing.

It is widely believed that sensory systems are optimized for processing stimuli occurring in the natural environment. However, it remains unknown whether this principle applies to the vestibular system, which contributes to essential brain functions ranging from the most automatic reflexes to spatial perception and motor coordination. Here we quantified, for the first time, the statistics of natural vestibular inputs experienced by freely moving human subjects during typical everyday activities. Although previous studies have found that the power spectra of natural signals across sensory modalities decay as a power law (i.e., as 1/f(α)), we found that this did not apply to natural vestibular stimuli. Instead, power decreased slowly at lower and more rapidly at higher frequencies for all motion dimensions. We further establish that this unique stimulus structure is the result of active motion as well as passive biomechanical filtering occurring before any neural processing. Notably, the transition frequency (i.e., frequency at which power starts to decrease rapidly) was lower when subjects passively experienced sensory stimulation than when they actively controlled stimulation through their own movement. In contrast to signals measured at the head, the spectral content of externally generated (i.e., passive) environmental motion did follow a power law. Specifically, transformations caused by both motor control and biomechanics shape the statistics of natural vestibular stimuli before neural processing. We suggest that the unique structure of natural vestibular stimuli will have important consequences on the neural coding strategies used by this essential sensory system to represent self-motion in everyday life.

Large-scale analysis of perceptual odor data

It is a general problem in sensory processing to understand which aspect of the sensory input is relevant to perception. In olfaction, because of the high-dimensionality, and the difficulty in describing smells [1]. One of the core questions in olfaction is therefore the so-called structureodor relationships. A deeper understanding of olfaction should involve aspects of natural stimulus statistics, odorant properties, physiological responses, evolution, odor perception, and behavioral relevance. As a step towards computational analyses in this direction, I accumulated a database consisting of several hundred perceptual descriptors for several thousand odors by merging data from different publicly available sources. Preliminary results from this dataset based on unsupervised and unsupervised methods are presented here. These preliminary results could give a better idea of the dimensionality of the odor space, and of how to approach studies of structure-odor relationships. Acknowledgement: participation to this meeting was supported by an ECRO Travel Grant.

Statistical structure of speech sound classes is congruent with cochlear nucleus response properties

Natural sounds possess considerable statistical structure. Lewicki (2002, Nature Neurosci. 5(4), 356–363) used independent components analysis (ICA) to reveal the statistical structure of environmental sounds, animal vocalizations, and human speech. Each sound class exhibited distinct statistical properties, but filters that optimally encoded speech closely resembled response properties in the mammalian auditory nerve. This and other analyses of statistical properties of speech examine only global structure without considering systematic variability in different speech sound classes, while acoustic/phonetic analyses of these classes are agnostic to their statistical structure. Here, statistical structure was investigated in principled subdivisions of speech: consonants organized by manner of articulation, and vowels organized by vocal tract configuration. Analyses reveal systematic differences for local statistical structure in speech: statistically optimal filters in ICA were highly diverse for different consonant classes but broadly similar for different vowel classes. While the global statistical structure of speech reflects auditory nerve response properties (Lewicki, 2002), local statistical structure of speech sound classes is well-aligned with cochlear nucleus response properties. Results support theories of efficient coding, in which sensory systems adapt and evolve in order to efficiently capture natural stimulus statistics.