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1.  Population code in mouse V1 facilitates read-out of natural scenes through increased sparseness 
Nature neuroscience  2014;17(6):851-857.
The neural code is believed to have adapted to the statistical properties of the natural environment. However, the principles that govern the organization of ensemble activity in the visual cortex during natural visual input are unknown. We recorded populations of up to 500 neurons in the mouse primary visual cortex and characterized the structure of their activity, comparing responses to natural movies with those to control stimuli. We found that higher-order correlations in natural scenes induce a sparser code, in which information is encoded by reliable activation of a smaller set of neurons and can be read-out more easily. This computationally advantageous encoding for natural scenes was state-dependent and apparent only in anesthetized and active awake animals, but not during quiet wakefulness. Our results argue for a functional benefit of sparsification that could be a general principle governing the structure of the population activity throughout cortical microcircuits.
doi:10.1038/nn.3707
PMCID: PMC4106281  PMID: 24747577
2.  The reliability of WorkWell Systems Functional Capacity Evaluation: a systematic review 
Background
Functional capacity evaluation (FCE) determines a person’s ability to perform work-related tasks and is a major component of the rehabilitation process. The WorkWell Systems (WWS) FCE (formerly known as Isernhagen Work Systems FCE) is currently the most commonly used FCE tool in German rehabilitation centres. Our systematic review investigated the inter-rater, intra-rater and test-retest reliability of the WWS FCE.
Methods
We performed a systematic literature search of studies on the reliability of the WWS FCE and extracted item-specific measures of inter-rater, intra-rater and test-retest reliability from the identified studies. Intraclass correlation coefficients ≥ 0.75, percentages of agreement ≥ 80%, and kappa coefficients ≥ 0.60 were categorised as acceptable, otherwise they were considered non-acceptable. The extracted values were summarised for the five performance categories of the WWS FCE, and the results were classified as either consistent or inconsistent.
Results
From 11 identified studies, 150 item-specific reliability measures were extracted. 89% of the extracted inter-rater reliability measures, all of the intra-rater reliability measures and 96% of the test-retest reliability measures of the weight handling and strength tests had an acceptable level of reliability, compared to only 67% of the test-retest reliability measures of the posture/mobility tests and 56% of the test-retest reliability measures of the locomotion tests. Both of the extracted test-retest reliability measures of the balance test were acceptable.
Conclusions
Weight handling and strength tests were found to have consistently acceptable reliability. Further research is needed to explore the reliability of the other tests as inconsistent findings or a lack of data prevented definitive conclusions.
doi:10.1186/1471-2474-15-106
PMCID: PMC3974446  PMID: 24674029
Functional capacity evaluation; Assessment; Reliability; Systematic review; WorkWell Systems; Isernhagen
3.  Slowness and Sparseness Have Diverging Effects on Complex Cell Learning 
PLoS Computational Biology  2014;10(3):e1003468.
Following earlier studies which showed that a sparse coding principle may explain the receptive field properties of complex cells in primary visual cortex, it has been concluded that the same properties may be equally derived from a slowness principle. In contrast to this claim, we here show that slowness and sparsity drive the representations towards substantially different receptive field properties. To do so, we present complete sets of basis functions learned with slow subspace analysis (SSA) in case of natural movies as well as translations, rotations, and scalings of natural images. SSA directly parallels independent subspace analysis (ISA) with the only difference that SSA maximizes slowness instead of sparsity. We find a large discrepancy between the filter shapes learned with SSA and ISA. We argue that SSA can be understood as a generalization of the Fourier transform where the power spectrum corresponds to the maximally slow subspace energies in SSA. Finally, we investigate the trade-off between slowness and sparseness when combined in one objective function.
Author Summary
A key question in visual neuroscience is how neural representations achieve invariance against appearance changes of objects. In particular, the invariance of complex cell responses in primary visual cortex against small translations is commonly interpreted as a signature of an invariant coding strategy possibly originating from an unsupervised learning principle. Various models have been proposed to explain the response properties of complex cells using a sparsity or a slowness criterion and it has been concluded that physiologically plausible receptive field properties can be derived from either criterion. Here, we show that the effect of the two objectives on the resulting receptive field properties is in fact very different. We conclude that slowness alone cannot explain the filter shapes of complex cells and discuss what kind of experimental measurements could help us to better asses the role of slowness and sparsity for complex cell representations.
doi:10.1371/journal.pcbi.1003468
PMCID: PMC3945087  PMID: 24603197
4.  Beyond GLMs: A Generative Mixture Modeling Approach to Neural System Identification 
PLoS Computational Biology  2013;9(11):e1003356.
Generalized linear models (GLMs) represent a popular choice for the probabilistic characterization of neural spike responses. While GLMs are attractive for their computational tractability, they also impose strong assumptions and thus only allow for a limited range of stimulus-response relationships to be discovered. Alternative approaches exist that make only very weak assumptions but scale poorly to high-dimensional stimulus spaces. Here we seek an approach which can gracefully interpolate between the two extremes. We extend two frequently used special cases of the GLM—a linear and a quadratic model—by assuming that the spike-triggered and non-spike-triggered distributions can be adequately represented using Gaussian mixtures. Because we derive the model from a generative perspective, its components are easy to interpret as they correspond to, for example, the spike-triggered distribution and the interspike interval distribution. The model is able to capture complex dependencies on high-dimensional stimuli with far fewer parameters than other approaches such as histogram-based methods. The added flexibility comes at the cost of a non-concave log-likelihood. We show that in practice this does not have to be an issue and the mixture-based model is able to outperform generalized linear and quadratic models.
Author Summary
An essential goal of sensory systems neuroscience is to characterize the functional relationship between neural responses and external stimuli. Of particular interest are the nonlinear response properties of single cells. Inherently linear approaches such as generalized linear modeling can nevertheless be used to fit nonlinear behavior by choosing an appropriate feature space for the stimulus. This requires, however, that one has already obtained a good understanding of a cells nonlinear properties, whereas more flexible approaches are necessary for the characterization of unexpected nonlinear behavior. In this work, we present a generalization of some frequently used generalized linear models which enables us to automatically extract complex stimulus-response relationships from recorded data. We show that our model can lead to substantial quantitative and qualitative improvements over generalized linear and quadratic models, which we illustrate on the example of primary afferents of the rat whisker system.
doi:10.1371/journal.pcbi.1003356
PMCID: PMC3836720  PMID: 24278006
5.  A fast and simple population code for orientation in primate V1 
Orientation tuning has been a classic model for understanding single neuron computation in the neocortex. However, little is known about how orientation can be read out from the activity of neural populations, in particular in alert animals. Our study is a first step towards that goal. We recorded from up to 20 well-isolated single neurons in the primary visual cortex of alert macaques simultaneously and applied a simple, neurally plausible decoder to read out the population code. We focus on two questions: First, what are the time course and the time scale at which orientation can be read out from the population response? Second, how complex does the decoding mechanism in a downstream neuron have to be in order to reliably discriminate between visual stimuli with different orientations? We show that the neural ensembles in primary visual cortex of awake macaques represent orientation in a way that facilitates a fast and simple read-out mechanism: with an average latency of 30–80 ms, the population code can be read out instantaneously with a short integration time of only tens of milliseconds and neither stimulus contrast nor correlations need to be taken into account to compute the optimal synaptic weight pattern. Our study shows that – similar to the case of single neuron computation – the representation of orientation in the spike patterns of neural populations can serve as an exemplary case for understanding of the computations performed by neural ensembles underlying visual processing during behavior.
doi:10.1523/JNEUROSCI.1335-12.2012
PMCID: PMC3506189  PMID: 22855811
6.  Temporal Adaptation Enhances Efficient Contrast Gain Control on Natural Images 
PLoS Computational Biology  2013;9(1):e1002889.
Divisive normalization in primary visual cortex has been linked to adaptation to natural image statistics in accordance to Barlow's redundancy reduction hypothesis. Using recent advances in natural image modeling, we show that the previously studied static model of divisive normalization is rather inefficient in reducing local contrast correlations, but that a simple temporal contrast adaptation mechanism of the half-saturation constant can substantially increase its efficiency. Our findings reveal the experimentally observed temporal dynamics of divisive normalization to be critical for redundancy reduction.
Author Summary
The redundancy reduction hypothesis postulates that neural representations adapt to sensory input statistics such that their responses become as statistically independent as possible. Based on this hypothesis, many properties of early visual neurons—like orientation selectivity or divisive normalization—have been linked to natural image statistics. Divisive normalization, in particular, models a widely observed neural response property: The divisive inhibition of a single neuron by a pool of others. This mechanism has been shown to reduce the redundancy among neural responses to typical contrast dependencies in natural images. Here, we show that the standard model of divisive normalization achieves substantially less redundancy reduction than a theoretically optimal mechanism called radial factorization. On the other hand, we find that radial factorization is inconsistent with existing neurophysiological observations. As a solution we suggest a new physiologically plausible modification of the standard model which accounts for the dynamics of the visual input by adapting to local contrasts during fixations. In this way the dynamic version of the standard model achieves almost optimal redundancy reduction performance. Our results imply that the dynamics of natural viewing conditions are critical for testing the role of divisive normalization for redundancy reduction.
doi:10.1371/journal.pcbi.1002889
PMCID: PMC3561086  PMID: 23382664
7.  How Sensitive Is the Human Visual System to the Local Statistics of Natural Images? 
PLoS Computational Biology  2013;9(1):e1002873.
A key hypothesis in sensory system neuroscience is that sensory representations are adapted to the statistical regularities in sensory signals and thereby incorporate knowledge about the outside world. Supporting this hypothesis, several probabilistic models of local natural image regularities have been proposed that reproduce neural response properties. Although many such physiological links have been made, these models have not been linked directly to visual sensitivity. Previous psychophysical studies of sensitivity to natural image regularities focus on global perception of large images, but much less is known about sensitivity to local natural image regularities. We present a new paradigm for controlled psychophysical studies of local natural image regularities and compare how well such models capture perceptually relevant image content. To produce stimuli with precise statistics, we start with a set of patches cut from natural images and alter their content to generate a matched set whose joint statistics are equally likely under a probabilistic natural image model. The task is forced choice to discriminate natural patches from model patches. The results show that human observers can learn to discriminate the higher-order regularities in natural images from those of model samples after very few exposures and that no current model is perfect for patches as small as 5 by 5 pixels or larger. Discrimination performance was accurately predicted by model likelihood, an information theoretic measure of model efficacy, indicating that the visual system possesses a surprisingly detailed knowledge of natural image higher-order correlations, much more so than current image models. We also perform three cue identification experiments to interpret how model features correspond to perceptually relevant image features.
Author Summary
Several aspects of primate visual physiology have been identified as adaptations to local regularities of natural images. However, much less work has measured visual sensitivity to local natural image regularities. Most previous work focuses on global perception of large images and shows that observers are more sensitive to visual information when image properties resemble those of natural images. In this work we measure human sensitivity to local natural image regularities using stimuli generated by patch-based probabilistic natural image models that have been related to primate visual physiology. We find that human observers can learn to discriminate the statistical regularities of natural image patches from those represented by current natural image models after very few exposures and that discriminability depends on the degree of regularities captured by the model. The quick learning we observed suggests that the human visual system is biased for processing natural images, even at very fine spatial scales, and that it has a surprisingly large knowledge of the regularities in natural images, at least in comparison to the state-of-the-art statistical models of natural images.
doi:10.1371/journal.pcbi.1002873
PMCID: PMC3554546  PMID: 23358106
8.  Functional analysis of ultra high information rates conveyed by rat vibrissal primary afferents 
Sensory receptors determine the type and the quantity of information available for perception. Here, we quantified and characterized the information transferred by primary afferents in the rat whisker system using neural system identification. Quantification of “how much” information is conveyed by primary afferents, using the direct method (DM), a classical information theoretic tool, revealed that primary afferents transfer huge amounts of information (up to 529 bits/s). Information theoretic analysis of instantaneous spike-triggered kinematic stimulus features was used to gain functional insight on “what” is coded by primary afferents. Amongst the kinematic variables tested—position, velocity, and acceleration—primary afferent spikes encoded velocity best. The other two variables contributed to information transfer, but only if combined with velocity. We further revealed three additional characteristics that play a role in information transfer by primary afferents. Firstly, primary afferent spikes show preference for well separated multiple stimuli (i.e., well separated sets of combinations of the three instantaneous kinematic variables). Secondly, neurons are sensitive to short strips of the stimulus trajectory (up to 10 ms pre-spike time), and thirdly, they show spike patterns (precise doublet and triplet spiking). In order to deal with these complexities, we used a flexible probabilistic neuron model fitting mixtures of Gaussians to the spike triggered stimulus distributions, which quantitatively captured the contribution of the mentioned features and allowed us to achieve a full functional analysis of the total information rate indicated by the DM. We found that instantaneous position, velocity, and acceleration explained about 50% of the total information rate. Adding a 10 ms pre-spike interval of stimulus trajectory achieved 80–90%. The final 10–20% were found to be due to non-linear coding by spike bursts.
doi:10.3389/fncir.2013.00190
PMCID: PMC3852094  PMID: 24367295
rat; whisker; vibrissae; primary afferents; tactile coding; information theory; spike-triggered mixture model
9.  Effort-reward imbalance and work ability: cross-sectional and longitudinal findings from the Second German Sociomedical Panel of Employees 
BMC Public Health  2012;12:875.
Background
Although data from longitudinal studies are sparse, effort-reward imbalance (ERI) seems to affect work ability. However, the potential pathway from restricted work ability to ERI must also be considered. Therefore, the aim of our study was to analyse cross-sectional and longitudinal associations between ERI and work ability and vice versa.
Methods
Data come from the Second German Sociomedical Panel of Employees. Logistic regression models were estimated to determine cross-sectional and longitudinal associations. The sample used to predict new cases of poor or moderate work ability was restricted to cases with good or excellent work ability at baseline. The sample used to predict new cases of ERI was restricted to persons without ERI at baseline.
Results
The cross-sectional analysis included 1501 full-time employed persons. The longitudinal analyses considered 600 participants with good or excellent baseline work ability and 666 participants without baseline ERI, respectively. After adjustment for socio-demographic variables, health-related behaviour and factors of the work environment, ERI was cross-sectionally associated with poor or moderate work ability (OR = 1.980; 95% CI: 1.428 to 2.747). Longitudinally, persons with ERI had 2.1 times higher odds of poor or moderate work ability after one year (OR = 2.093; 95% CI: 1.047 to 4.183). Conversely, persons with poor or moderate work ability had 2.6 times higher odds of an ERI after one year (OR = 2.573; 95% CI: 1.314 to 5.041).
Conclusions
Interventions that enable workers to cope with ERI or address indicators of ERI directly could promote the maintenance of work ability. Integration management programmes for persons with poor work ability should also consider their psychosocial demands.
doi:10.1186/1471-2458-12-875
PMCID: PMC3505747  PMID: 23067110
10.  Mixtures of Conditional Gaussian Scale Mixtures Applied to Multiscale Image Representations 
PLoS ONE  2012;7(7):e39857.
We present a probabilistic model for natural images that is based on mixtures of Gaussian scale mixtures and a simple multiscale representation. We show that it is able to generate images with interesting higher-order correlations when trained on natural images or samples from an occlusion-based model. More importantly, our multiscale model allows for a principled evaluation. While it is easy to generate visually appealing images, we demonstrate that our model also yields the best performance reported to date when evaluated with respect to the cross-entropy rate, a measure tightly linked to the average log-likelihood. The ability to quantitatively evaluate our model differentiates it from other multiscale models, for which evaluation of these kinds of measures is usually intractable.
doi:10.1371/journal.pone.0039857
PMCID: PMC3409213  PMID: 22859943
11.  A New Perceptual Bias Reveals Suboptimal Population Decoding of Sensory Responses 
PLoS Computational Biology  2012;8(4):e1002453.
Several studies have reported optimal population decoding of sensory responses in two-alternative visual discrimination tasks. Such decoding involves integrating noisy neural responses into a more reliable representation of the likelihood that the stimuli under consideration evoked the observed responses. Importantly, an ideal observer must be able to evaluate likelihood with high precision and only consider the likelihood of the two relevant stimuli involved in the discrimination task. We report a new perceptual bias suggesting that observers read out the likelihood representation with remarkably low precision when discriminating grating spatial frequencies. Using spectrally filtered noise, we induced an asymmetry in the likelihood function of spatial frequency. This manipulation mainly affects the likelihood of spatial frequencies that are irrelevant to the task at hand. Nevertheless, we find a significant shift in perceived grating frequency, indicating that observers evaluate likelihoods of a broad range of irrelevant frequencies and discard prior knowledge of stimulus alternatives when performing two-alternative discrimination.
Author Summary
An attractive view on human information processing proposes that inference problems are dealt with in a statistically optimal fashion. This hypothesis can explain aspects of perception, movement planning, cognition and decision making. In the present study, I use a new psychophysical paradigm that reveals surprisingly suboptimal perceptual decision making. Observers discriminate between two sinusoidal gratings of a different spatial frequency. Making use of visual noise, I induce an asymmetry in neural population responses to the gratings and find this asymmetry to effectively bias perceptual decision making. A simple ideal observer model, uninformed about the presence of visual noise but only considering the two grating spatial frequencies relevant to the task at hand, manages to avoid such a bias. I conclude that observers are limited in their ability to make use of prior knowledge of relevant visual features when performing this task. These results are in line with a growing number of findings suggesting that near-optimal decoders, although straightforward to implement and achieving near-maximal performance, consistently overestimate empirical performance in simple perceptual tasks.
doi:10.1371/journal.pcbi.1002453
PMCID: PMC3325184  PMID: 22511853
12.  The effect of noise correlations in populations of diversely tuned neurons 
The amount of information encoded by networks of neurons critically depends on the correlation structure of their activity. Neurons with similar stimulus preferences tend to have higher noise correlations than others. In homogeneous populations of neurons this limited range correlation structure is highly detrimental to the accuracy of a population code. Therefore, reduced spike count correlations under attention, after adaptation or after learning have been interpreted as evidence for a more efficient population code. Here we analyze the role of limited range correlations in more realistic, heterogeneous population models. We use Fisher information and maximum likelihood decoding to show that reduced correlations do not necessarily improve encoding accuracy. In fact, in populations with more than a few hundred neurons, increasing the level of limited range correlations can substantially improve encoding accuracy. We found that this improvement results from a decrease in noise entropy that is associated with increasing correlations if the marginal distributions are unchanged. Surprisingly, for constant noise entropy and in the limit of large populations the encoding accuracy is independent of both structure and magnitude of noise correlations.
doi:10.1523/JNEUROSCI.2539-11.2011
PMCID: PMC3221941  PMID: 21976512
13.  Reconstructing Stimuli from the Spike Times of Leaky Integrate and Fire Neurons 
Reconstructing stimuli from the spike trains of neurons is an important approach for understanding the neural code. One of the difficulties associated with this task is that signals which are varying continuously in time are encoded into sequences of discrete events or spikes. An important problem is to determine how much information about the continuously varying stimulus can be extracted from the time-points at which spikes were observed, especially if these time-points are subject to some sort of randomness. For the special case of spike trains generated by leaky integrate and fire neurons, noise can be introduced by allowing variations in the threshold every time a spike is released. A simple decoding algorithm previously derived for the noiseless case can be extended to the stochastic case, but turns out to be biased. Here, we review a solution to this problem, by presenting a simple yet efficient algorithm which greatly reduces the bias, and therefore leads to better decoding performance in the stochastic case.
doi:10.3389/fnins.2011.00001
PMCID: PMC3046364  PMID: 21390287
decoding; spiking neurons; Bayesian inference; population coding; leaky integrate and fire
15.  Bayesian Inference for Generalized Linear Models for Spiking Neurons 
Generalized Linear Models (GLMs) are commonly used statistical methods for modelling the relationship between neural population activity and presented stimuli. When the dimension of the parameter space is large, strong regularization has to be used in order to fit GLMs to datasets of realistic size without overfitting. By imposing properly chosen priors over parameters, Bayesian inference provides an effective and principled approach for achieving regularization. Here we show how the posterior distribution over model parameters of GLMs can be approximated by a Gaussian using the Expectation Propagation algorithm. In this way, we obtain an estimate of the posterior mean and posterior covariance, allowing us to calculate Bayesian confidence intervals that characterize the uncertainty about the optimal solution. From the posterior we also obtain a different point estimate, namely the posterior mean as opposed to the commonly used maximum a posteriori estimate. We systematically compare the different inference techniques on simulated as well as on multi-electrode recordings of retinal ganglion cells, and explore the effects of the chosen prior and the performance measure used. We find that good performance can be achieved by choosing an Laplace prior together with the posterior mean estimate.
doi:10.3389/fncom.2010.00012
PMCID: PMC2889714  PMID: 20577627
spiking neurons; Bayesian inference; population coding; sparsity; multielectrode recordings; receptive field; GLM; functional connectivity
16.  Natural Image Coding in V1: How Much Use Is Orientation Selectivity? 
PLoS Computational Biology  2009;5(4):e1000336.
Orientation selectivity is the most striking feature of simple cell coding in V1 that has been shown to emerge from the reduction of higher-order correlations in natural images in a large variety of statistical image models. The most parsimonious one among these models is linear Independent Component Analysis (ICA), whereas second-order decorrelation transformations such as Principal Component Analysis (PCA) do not yield oriented filters. Because of this finding, it has been suggested that the emergence of orientation selectivity may be explained by higher-order redundancy reduction. To assess the tenability of this hypothesis, it is an important empirical question how much more redundancy can be removed with ICA in comparison to PCA or other second-order decorrelation methods. Although some previous studies have concluded that the amount of higher-order correlation in natural images is generally insignificant, other studies reported an extra gain for ICA of more than 100%. A consistent conclusion about the role of higher-order correlations in natural images can be reached only by the development of reliable quantitative evaluation methods. Here, we present a very careful and comprehensive analysis using three evaluation criteria related to redundancy reduction: In addition to the multi-information and the average log-loss, we compute complete rate–distortion curves for ICA in comparison with PCA. Without exception, we find that the advantage of the ICA filters is small. At the same time, we show that a simple spherically symmetric distribution with only two parameters can fit the data significantly better than the probabilistic model underlying ICA. This finding suggests that, although the amount of higher-order correlation in natural images can in fact be significant, the feature of orientation selectivity does not yield a large contribution to redundancy reduction within the linear filter bank models of V1 simple cells.
Author Summary
Since the Nobel Prize winning work of Hubel and Wiesel it has been known that orientation selectivity is an important feature of simple cells in the primary visual cortex. The standard description of this stage of visual processing is that of a linear filter bank where each neuron responds to an oriented edge at a certain location within the visual field. From a vision scientist's point of view, we would like to understand why an orientation selective filter bank provides a useful image representation. Several previous studies have shown that orientation selectivity arises when the individual filter shapes are optimized according to the statistics of natural images. Here, we investigate quantitatively how critical the feature of orientation selectivity is for this optimization. We find that there is a large range of non-oriented filter shapes that perform nearly as well as the optimal orientation selective filters. We conclude that the standard filter bank model is not suitable to reveal a strong link between orientation selectivity and the statistics of natural images. Thus, to understand the role of orientation selectivity in the primary visual cortex, we will have to develop more sophisticated, nonlinear models of natural images.
doi:10.1371/journal.pcbi.1000336
PMCID: PMC2658886  PMID: 19343216
17.  Bayesian Population Decoding of Spiking Neurons 
The timing of action potentials in spiking neurons depends on the temporal dynamics of their inputs and contains information about temporal fluctuations in the stimulus. Leaky integrate-and-fire neurons constitute a popular class of encoding models, in which spike times depend directly on the temporal structure of the inputs. However, optimal decoding rules for these models have only been studied explicitly in the noiseless case. Here, we study decoding rules for probabilistic inference of a continuous stimulus from the spike times of a population of leaky integrate-and-fire neurons with threshold noise. We derive three algorithms for approximating the posterior distribution over stimuli as a function of the observed spike trains. In addition to a reconstruction of the stimulus we thus obtain an estimate of the uncertainty as well. Furthermore, we derive a ‘spike-by-spike’ online decoding scheme that recursively updates the posterior with the arrival of each new spike. We use these decoding rules to reconstruct time-varying stimuli represented by a Gaussian process from spike trains of single neurons as well as neural populations.
doi:10.3389/neuro.10.021.2009
PMCID: PMC2790948  PMID: 20011217
Bayesian decoding; population coding; spiking neurons; approximate inference

Results 1-17 (17)